Significance and Roles of Proteus spp. Bacteria in Natural Environments
Identifieur interne : 000105 ( Pmc/Corpus ); précédent : 000104; suivant : 000106Significance and Roles of Proteus spp. Bacteria in Natural Environments
Auteurs : Dominika DrzewieckaSource :
- Microbial Ecology [ 0095-3628 ] ; 2016.
Abstract
Url:
DOI: 10.1007/s00248-015-0720-6
PubMed: 26748500
PubMed Central: 5080321
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PMC:5080321Le document en format XML
<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">Significance and Roles of <italic>Proteus</italic> spp. Bacteria in Natural Environments</title><author><name sortKey="Drzewiecka, Dominika" sort="Drzewiecka, Dominika" uniqKey="Drzewiecka D" first="Dominika" last="Drzewiecka">Dominika Drzewiecka</name><affiliation><nlm:aff id="Aff1">Department of General Microbiology, Institute of Microbiology, Biotechnology and Immunology, University of Łódź, 90-237 Łódź, Poland</nlm:aff></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">26748500</idno><idno type="pmc">5080321</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5080321</idno><idno type="RBID">PMC:5080321</idno><idno type="doi">10.1007/s00248-015-0720-6</idno><date when="2016">2016</date><idno type="wicri:Area/Pmc/Corpus">000105</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Corpus" wicri:corpus="PMC">000105</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Significance and Roles of <italic>Proteus</italic> spp. Bacteria in Natural Environments</title><author><name sortKey="Drzewiecka, Dominika" sort="Drzewiecka, Dominika" uniqKey="Drzewiecka D" first="Dominika" last="Drzewiecka">Dominika Drzewiecka</name><affiliation><nlm:aff id="Aff1">Department of General Microbiology, Institute of Microbiology, Biotechnology and Immunology, University of Łódź, 90-237 Łódź, Poland</nlm:aff></affiliation></author></analytic><series><title level="j">Microbial Ecology</title><idno type="ISSN">0095-3628</idno><idno type="eISSN">1432-184X</idno><imprint><date when="2016">2016</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p><italic>Proteus</italic> spp. bacteria were first described in 1885 by Gustav Hauser, who had revealed their feature of intensive swarming growth. Currently, the genus is divided into <italic>Proteus mirabilis</italic>, <italic>Proteus vulgaris</italic>, <italic>Proteus penneri</italic>, <italic>Proteus hauseri</italic>, and three unnamed genomospecies 4, 5, and 6 and consists of 80 O-antigenic serogroups. The bacteria are known to be human opportunistic pathogens, isolated from urine, wounds, and other clinical sources. It is postulated that intestines are a reservoir of these proteolytic organisms. Many wild and domestic animals may be hosts of <italic>Proteus</italic> spp. bacteria, which are commonly known to play a role of parasites or commensals. However, interesting examples of their symbiotic relationships with higher organisms have also been described. <italic>Proteus</italic> spp. bacteria present in soil or water habitats are often regarded as indicators of fecal pollution, posing a threat of poisoning when the contaminated water or seafood is consumed. The health risk may also be connected with drug-resistant strains sourcing from intestines. Positive aspects of the bacteria presence in water and soil are connected with exceptional features displayed by autochthonic <italic>Proteus</italic> spp. strains detected in these environments. These rods acquire various metabolic abilities allowing their adaptation to different environmental conditions, such as high concentrations of heavy metals or toxic substances, which may be exploited as sources of energy and nutrition by the bacteria. The <italic>Proteus</italic> spp. abilities to tolerate or utilize polluting compounds as well as promote plant growth provide a possibility of employing these microorganisms in bioremediation and environmental protection.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Aboh, Ea" uniqKey="Aboh E">EA Aboh</name></author><author><name sortKey="Giwa, Fj" uniqKey="Giwa F">FJ Giwa</name></author><author><name sortKey="Giwa, A" uniqKey="Giwa A">A Giwa</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Abu Samra, Mt" uniqKey="Abu Samra M">MT Abu-Samra</name></author><author><name sortKey="Shuaib, Ya" uniqKey="Shuaib Y">YA Shuaib</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Akoachere, J Ftk" uniqKey="Akoachere J">J-FTK Akoachere</name></author><author><name sortKey="Oben, Pm" uniqKey="Oben P">PM Oben</name></author><author><name sortKey="Mbivnjo, Bs" uniqKey="Mbivnjo 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<front><journal-meta><journal-id journal-id-type="nlm-ta">Microb Ecol</journal-id><journal-id journal-id-type="iso-abbrev">Microb. Ecol</journal-id><journal-title-group><journal-title>Microbial Ecology</journal-title></journal-title-group><issn pub-type="ppub">0095-3628</issn><issn pub-type="epub">1432-184X</issn><publisher><publisher-name>Springer US</publisher-name><publisher-loc>New York</publisher-loc></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">26748500</article-id><article-id pub-id-type="pmc">5080321</article-id><article-id pub-id-type="publisher-id">720</article-id><article-id pub-id-type="doi">10.1007/s00248-015-0720-6</article-id><article-categories><subj-group subj-group-type="heading"><subject>Minireviews</subject></subj-group></article-categories><title-group><article-title>Significance and Roles of <italic>Proteus</italic> spp. Bacteria in Natural Environments</article-title></title-group><contrib-group><contrib contrib-type="author" corresp="yes"><name><surname>Drzewiecka</surname><given-names>Dominika</given-names></name><address><phone>+48-42-6354469</phone><email>domkam@biol.uni.lodz.pl</email></address><xref ref-type="aff" rid="Aff1"></xref></contrib><aff id="Aff1">Department of General Microbiology, Institute of Microbiology, Biotechnology and Immunology, University of Łódź, 90-237 Łódź, Poland</aff></contrib-group><pub-date pub-type="epub"><day>9</day><month>1</month><year>2016</year></pub-date><pub-date pub-type="pmc-release"><day>9</day><month>1</month><year>2016</year></pub-date><pub-date pub-type="ppub"><year>2016</year></pub-date><volume>72</volume><issue>4</issue><fpage>741</fpage><lpage>758</lpage><history><date date-type="received"><day>22</day><month>7</month><year>2015</year></date><date date-type="accepted"><day>13</day><month>12</month><year>2015</year></date></history><permissions><copyright-statement>© The Author(s) 2016</copyright-statement><license license-type="OpenAccess"><license-p><bold>Open Access</bold> This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.</license-p></license></permissions><abstract id="Abs1"><p><italic>Proteus</italic> spp. bacteria were first described in 1885 by Gustav Hauser, who had revealed their feature of intensive swarming growth. Currently, the genus is divided into <italic>Proteus mirabilis</italic>, <italic>Proteus vulgaris</italic>, <italic>Proteus penneri</italic>, <italic>Proteus hauseri</italic>, and three unnamed genomospecies 4, 5, and 6 and consists of 80 O-antigenic serogroups. The bacteria are known to be human opportunistic pathogens, isolated from urine, wounds, and other clinical sources. It is postulated that intestines are a reservoir of these proteolytic organisms. Many wild and domestic animals may be hosts of <italic>Proteus</italic> spp. bacteria, which are commonly known to play a role of parasites or commensals. However, interesting examples of their symbiotic relationships with higher organisms have also been described. <italic>Proteus</italic> spp. bacteria present in soil or water habitats are often regarded as indicators of fecal pollution, posing a threat of poisoning when the contaminated water or seafood is consumed. The health risk may also be connected with drug-resistant strains sourcing from intestines. Positive aspects of the bacteria presence in water and soil are connected with exceptional features displayed by autochthonic <italic>Proteus</italic> spp. strains detected in these environments. These rods acquire various metabolic abilities allowing their adaptation to different environmental conditions, such as high concentrations of heavy metals or toxic substances, which may be exploited as sources of energy and nutrition by the bacteria. The <italic>Proteus</italic> spp. abilities to tolerate or utilize polluting compounds as well as promote plant growth provide a possibility of employing these microorganisms in bioremediation and environmental protection.</p></abstract><kwd-group xml:lang="en"><title>Keywords</title><kwd>Natural microflora</kwd><kwd>Symbionts</kwd><kwd>Pathogens</kwd><kwd>Fecal pollution</kwd><kwd>Bioremediation</kwd><kwd>PGPR</kwd></kwd-group><custom-meta-group><custom-meta><meta-name>issue-copyright-statement</meta-name><meta-value>© Springer Science+Business Media New York 2016</meta-value></custom-meta></custom-meta-group></article-meta></front><body><sec id="Sec1"><title>Introduction</title><sec id="Sec2"><title><italic>Proteus</italic> Like in Homer’s Poem…</title><p>Microorganisms belonging to the genus <italic>Proteus</italic> were first described in 1885 by a German microbiologist Gustav Hauser, who had revealed their ability to swarm on solid surfaces. The name <italic>Proteus</italic> came from Homer’s “Odyssey” and its character Proteus, who could change his shape and had an ability of endless transformation. Hauser described two species of the genus: <italic>Proteus vulgaris</italic> and <italic>Proteus mirabilis</italic> [<xref ref-type="bibr" rid="CR81">81</xref>]. The swarming ability, connected with a change of short swimmer cells into long, poli-nucleous and hyper-flagellated swarmer cells, is especially visible in the second species. This is a possible source of the name of <italic>P. mirabilis</italic>, which in Latin means amazing, marvelous, splendid. Hauser might have considered <italic>P. vulgaris</italic> to be more common and ordinary; therefore, he gave it the Latin name meaning widespread, usual. The ability of swarming growth is used in a simple and effective Dienes test to differentiate <italic>Proteus</italic> spp. strains with discriminatory power comparable to ribotyping [<xref ref-type="bibr" rid="CR114">114</xref>]. The phenomenon described by Dienes in 1946 consists in forming boundaries between the swarming growth of different strains, while isogenic strains merge with each other (Fig. <xref rid="Fig1" ref-type="fig">1</xref>). However, the background of the expression of the territorial competition between two swarming non-isogenic strains still remains unclear [<xref ref-type="bibr" rid="CR8">8</xref>, <xref ref-type="bibr" rid="CR48">48</xref>]. The formation of the boundaries (Dienes lines) may depend on different profiles of produced proticines (<italic>Proteus</italic> bacteriocines) and different profiles of strain sensitivity [<xref ref-type="bibr" rid="CR129">129</xref>]. Budding et al. [<xref ref-type="bibr" rid="CR19">19</xref>] suggested that one of the meeting strains dominated over the other killing it in the cell–cell contact because round dead cells were observed near the border in the swarm of the dominated strain. The Dienes reaction is connected with at least three recognized gene clusters enabling the self-recognition of <italic>P. mirabilis</italic> bacteria. Two of them (<italic>idr</italic> and <italic>tss</italic>) encode cytotoxins and a type VI secretion system, respectively [<xref ref-type="bibr" rid="CR151">151</xref>], while the third one (<italic>ids</italic>) encodes the Ids proteins responsible for self-identification [<xref ref-type="bibr" rid="CR21">21</xref>, <xref ref-type="bibr" rid="CR49">49</xref>]. However, the mutation in the <italic>ids</italic> genes does not provoke the killing of parent or mutant strain cells, although the Dienes line is visible between their swarms [<xref ref-type="bibr" rid="CR48">48</xref>].<fig id="Fig1"><label>Fig. 1</label><caption><p><italic>P. mirabilis</italic> strains swarming on the surface of an agar plate: isogenic A and B (no line of demarcation is visible) versus unrelated C (clear Dienes line of demarcation)</p></caption><graphic xlink:href="248_2015_720_Fig1_HTML" id="MO1"></graphic></fig></p><p>The genus <italic>Proteus</italic> includes Gram-negative, facultative anaerobic, heterotrophic, and proteolytic rods being human opportunistic pathogens. The taxonomic classification of these bacteria has changed several times. Lately, the only <italic>Proteus</italic> species with no clinical significance, <italic>Proteus myxofaciens</italic>, has been postulated to be moved from the genus <italic>Proteus</italic> to a new genus <italic>Cosenzaea</italic> [<xref ref-type="bibr" rid="CR47">47</xref>]. Among other changes, the exclusion from the genus <italic>Proteus</italic> of several species that created new genera <italic>Providencia</italic> and <italic>Morganella</italic> is worth mentioning. These three closely related genera have formed the tribe <italic>Proteeae</italic> in the family <italic>Enterobacteriaceae</italic> [<xref ref-type="bibr" rid="CR81">81</xref>]. Currently, the genus <italic>Proteus</italic> consists of <italic>P. mirabilis</italic>, <italic>P. vulgaris</italic>, <italic>Proteus penneri</italic>, <italic>Proteus hauseri</italic>, and three genomospecies 4, 5, and 6. <italic>P. hauseri</italic> as well as the genomospecies were separated from <italic>P. vulgaris</italic> on the grounds of molecular studies and form <italic>P. vulgaris</italic> group. The genomospecies 4, 5, and 6 are marked only with numbers as there have been no metabolic properties indicated to allow their full differentiation [<xref ref-type="bibr" rid="CR104">104</xref>]. The main biochemical features typical of the genus and distinguishing <italic>Proteus</italic> species are summarized in Table <xref rid="Tab1" ref-type="table">1</xref>.<table-wrap id="Tab1"><label>Table 1</label><caption><p>The main metabolic characteristics of <italic>Proteus</italic> spp. [<xref ref-type="bibr" rid="CR103">103</xref>, <xref ref-type="bibr" rid="CR104">104</xref>]: “+”positive in 100 % strains; “−”negative in 100 % strains; in the other cases, the percentage of strains exhibiting positive reaction is given in parentheses</p></caption><table frame="hsides" rules="groups"><thead><tr><th>Feature</th><th><italic>P. mirabilis</italic></th><th><italic>P. penneri</italic></th><th><italic>P. vulgaris</italic></th><th><italic>P. hauseri</italic></th><th><italic>P.</italic> genomospecies 4, 5, and 6</th></tr></thead><tbody><tr><td colspan="6">Typical of the genus and distinguishing it from the other <italic>Enterobacteriaceae</italic></td></tr><tr><td>Phenylalanine deaminase<break></break>Lysine decarboxylation<break></break>Arginine hydrolysis<break></break>Urease production<break></break>Glucose fermentation<break></break>Mannose fermentation<break></break>Lactose fermentation<break></break>Methyl-red<break></break>Growth in KCN<break></break>Tyrosine clearing</td><td>+ (98 %)<break></break>−<break></break>−<break></break>+ (98 %)<break></break>+<break></break>−<break></break>− (2 %)<break></break>+ (97 %)<break></break>+ (98 %)<break></break>+ (91 %)</td><td>+ (99 %)<break></break>−<break></break>−<break></break>+<break></break>+<break></break>−<break></break>− (1 %)<break></break>+<break></break>+ (99 %)<break></break>+</td><td>+<break></break>−<break></break>−<break></break>+ (86 %)<break></break>+<break></break>−<break></break>−<break></break>+ (86 %)<break></break>+ (99 %)<break></break>+</td><td>+<break></break>−<break></break>−<break></break>+<break></break>+<break></break>−<break></break>−<break></break>+<break></break>+<break></break>+</td><td>+<break></break>−<break></break>−<break></break>+<break></break>+<break></break>−<break></break>−<break></break>+<break></break>+ (97 %)<break></break>+</td></tr><tr><td colspan="6">Typical of the species and allowing their differentiation</td></tr><tr><td>Ornithine decarboxylation<break></break>Indole production<break></break>Lipase production<break></break>DNase production<break></break>Maltose fermentation<break></break>Sucrose fermentation<break></break>Salicin fermentation<break></break>Esculin hydrolysis<break></break>Citrate utilization</td><td>+ (99 %)<break></break>− (2 %)<break></break>+ (92 %)<break></break>+/− (50 %)<break></break>−<break></break>− (15 %)<break></break>−<break></break>−<break></break>+ (65 %)</td><td>−<break></break>−<break></break>− (35 %)<break></break>− (12 %)<break></break>+ (96 %)<break></break>+<break></break>−<break></break>−<break></break>−</td><td>−<break></break>+<break></break>− (14 %)<break></break>+<break></break>+<break></break>+<break></break>+<break></break>+<break></break>− (29 %)</td><td>−<break></break>+<break></break>−<break></break>−<break></break>+<break></break>+<break></break>−<break></break>−<break></break>−</td><td>−<break></break>+<break></break>+ (97 %)<break></break>+ (85 %)<break></break>+<break></break>+<break></break>− (3 %)<break></break>− (3 %)<break></break>−</td></tr></tbody></table></table-wrap></p><p>Bacteria from the genus <italic>Proteus</italic> can also be differentiated on the basis of their O-antigen variability, although serotyping is not included in the routine diagnostics of these rods. So far, there have been established 80 O-antigenic serogroups in the genus, some of them divided into subgroups [<xref ref-type="bibr" rid="CR7">7</xref>, <xref ref-type="bibr" rid="CR67">67</xref>, <xref ref-type="bibr" rid="CR135">135</xref>], and many new O serotypes are still being discovered (D. Drzewiecka, unpublished data). The chemical structure of the sugar part of the lipopolysaccharide may play an important role in the adaptation of <italic>Proteus</italic> spp. bacteria to environmental conditions and enhancing their pathogenicity, as some O serotypes are more prevalent and more frequently isolated from clinical sources than the others (Table <xref rid="Tab2" ref-type="table">2</xref>) [<xref ref-type="bibr" rid="CR7">7</xref>, <xref ref-type="bibr" rid="CR35">35</xref>, <xref ref-type="bibr" rid="CR37">37</xref>, <xref ref-type="bibr" rid="CR72">72</xref>, <xref ref-type="bibr" rid="CR111">111</xref>, <xref ref-type="bibr" rid="CR133">133</xref>].<table-wrap id="Tab2"><label>Table 2</label><caption><p>Pathogenicity of <italic>Proteus</italic> spp. rods to humans [<xref ref-type="bibr" rid="CR7">7</xref>, <xref ref-type="bibr" rid="CR8">8</xref>, <xref ref-type="bibr" rid="CR35">35</xref>, <xref ref-type="bibr" rid="CR37">37</xref>, <xref ref-type="bibr" rid="CR72">72</xref>, <xref ref-type="bibr" rid="CR81">81</xref>, <xref ref-type="bibr" rid="CR111">111</xref>, <xref ref-type="bibr" rid="CR125">125</xref>, <xref ref-type="bibr" rid="CR133">133</xref>, <xref ref-type="bibr" rid="CR148">148</xref>]</p></caption><table frame="hsides" rules="groups"><thead><tr><th>Infections</th><th>Virulence factors</th><th>Prevalent O-serotypes</th></tr></thead><tbody><tr><td>• Urinary tract infections (cystitis, prostatitis, pyelonephritis, kidney stone formation)<break></break>• Wounds and burns infections, abscesses<break></break>• Respiratory tract infections<break></break>• Bacteremia<break></break>• Meningitis<break></break>• Intestine colonization (diarrhea)<break></break>• Nosocomial infections<break></break>• Rheumatoid arthritis (?) – autoaggressive antibodies may arise due to the molecular mimicry between <italic>Proteus</italic> hemolysin and urease, and human white blood cells</td><td>• Fimbriae – adhesion<break></break>• Flagella – swimming, swarming growth<break></break>• Urease – urine pH elevation, kidney stones formation<break></break>• LPS – endotoxin<break></break>• O and capsular polysaccharides – swarming facilitation, kidney stones and biofilm formation, serospecificity<break></break>• Biofilm – protection<break></break>• Invasiveness – internalization into host cells<break></break>• Haemolysins – cytotoxicity<break></break>• <italic>Proteus</italic> toxic agglutinin – cell–cell aggregation, cytotoxicity<break></break>• Proteases – antibodies degradation<break></break>• Deaminases – α-keto-acid siderophores production and iron acquisition<break></break>• Zinc and phosphate transport systems – utilization</td><td>• O3, O6, O10, O11, O13, O23, O24, O27, O28, O29, O30 – including <italic>P. mirabilis</italic> and <italic>P. vulgaris</italic> strains<break></break>• O17, O61, O64, O65 – including <italic>P. penneri</italic> strains mainly<break></break>• O78 – including <italic>P. mirabilis</italic> strains (data only from Poland)<break></break>• O79 including <italic>P.</italic> genomospecies strains (data only from Poland)</td></tr></tbody></table></table-wrap></p><p><italic>Proteus</italic> spp. bacteria have been isolated from different human and non-human environments and their presence in higher organisms, soil, and water is well documented. However, their specific features and roles played in their natural habitats have not been summarized so far.</p></sec></sec><sec id="Sec3"><title>Human Beings and <italic>Proteus</italic> Bacteria—Commensals and Parasites</title><p><italic>Proteus</italic> spp. bacteria are mostly known as opportunistic human pathogens. Their roles in the pathogenesis of human beings as well as their virulence factors enabling the bacteria to reach different niches of the host organism and survive have been extensively studied and reviewed [<xref ref-type="bibr" rid="CR8">8</xref>, <xref ref-type="bibr" rid="CR36">36</xref>, <xref ref-type="bibr" rid="CR81">81</xref>, <xref ref-type="bibr" rid="CR89">89</xref>, <xref ref-type="bibr" rid="CR103">103</xref>, <xref ref-type="bibr" rid="CR124">124</xref>, <xref ref-type="bibr" rid="CR125">125</xref>] and are summarized in Table <xref rid="Tab2" ref-type="table">2</xref>. The bacteria cause infections mainly in people with an impaired immunity system, and most all of them may be a source of complicated urinary tract and wound infections as well as nosocomial infections. Urinary tract infections are most frequently ascending, often connected with the presence of urinary catheters. It should be noticed that <italic>Proteus</italic> spp. are the most prevalent bacteria, isolated from bladder and kidney stones (70 % of cases). <italic>P. mirabilis</italic> is the main cause of all <italic>Proteus</italic> spp. infections accounting for 80–90 % of them.</p><p>It is postulated that human intestines are a reservoir of <italic>Proteus</italic> bacteria, especially those belonging to prevailing <italic>P. mirabilis</italic> species, and they are members of natural fecal microflora of several percent of human population [<xref ref-type="bibr" rid="CR124">124</xref>]. Lately, Porres-Osante et al. [<xref ref-type="bibr" rid="CR118">118</xref>] reported the presence of <italic>Proteus</italic> spp. bacteria (one <italic>P. mirabilis</italic> and one <italic>P. vulgaris</italic> strain) in fecal samples from 4 % of healthy Spanish volunteers. Zilberstein et al. [<xref ref-type="bibr" rid="CR160">160</xref>], using cultivation methods to study the microbiota in particular parts of the digestive tract, stated that <italic>Proteus</italic> spp. bacteria were absent from the mouth and the esophagus of healthy volunteers. However, the bacteria were present in comparatively high mean concentrations in the stomach of 8.1 % of volunteers (10<sup>5</sup> colony forming units (CFU)/mL), the duodenum (45.5 %, 10<sup>2</sup>), the proximal jejunum (45.5 %, 10<sup>4</sup>), the proximal ileum (20 %, 10<sup>6</sup>), the distal ileum (19 %, 10<sup>3.5</sup>), the cecum (12.5 %, 10<sup>4</sup>), the colon (ascending, 33.3 %, 10<sup>5</sup>; transverse, 37.5 %, 10<sup>5</sup>; descending, 25 %, 10<sup>5</sup>; and sigmoid, 34.8 %, 10<sup>7</sup>), and in the rectum (30 %, 10<sup>7</sup>). The other members of the family <italic>Enterobacteriaceae</italic>—<italic>Escherichia coli</italic>, <italic>Enterobacter</italic> spp., and <italic>Klebsiella</italic> spp.—were detected in the same places in the lower digestive tract, but they were more prevalent.</p><p><italic>Proteus</italic> spp. are regarded to be an undesired element of intestinal microflora, as the bacteria may also become a causative agent of diarrhea. Although Ikeobi et al. [<xref ref-type="bibr" rid="CR59">59</xref>] did not notice significant differences in the presence of <italic>Proteeae</italic> members in the intestines of healthy individuals and diarrheal patients, Müller [<xref ref-type="bibr" rid="CR91">91</xref>, <xref ref-type="bibr" rid="CR92">92</xref>] isolated <italic>P. mirabilis</italic> strains statistically more frequently from feces of patients suffering from diarrhea than from healthy individuals. The author suggested that the bacteria may become opportunists when the illness is caused by other intestinal pathogens or they may lead to intestinal disorders independently. Also, <italic>P. penneri</italic> strains were more frequently isolated from sick than from healthy people, while <italic>P. vulgaris</italic> were present in almost the same number of individuals in each group.</p><p>Thus, the presence of <italic>Proteus</italic> spp. bacteria in the gastrointestinal tract may also be treated as a carrier state, because in some conditions, it may lead to cross-infections and autoinfections especially in the urinary tract, which was observed many years ago by de Louvois [<xref ref-type="bibr" rid="CR73">73</xref>] using serotyping as well as the Dienes test and confirmed in other studies [<xref ref-type="bibr" rid="CR8">8</xref>, <xref ref-type="bibr" rid="CR48">48</xref>]. Chow et al. [<xref ref-type="bibr" rid="CR26">26</xref>] emphasized the role of the intestinal tract as a reservoir of <italic>P. mirabilis</italic> bacteria leading to person-to-person transmitted nosocomial infection. Drzewiecka et al. [<xref ref-type="bibr" rid="CR34">34</xref>, <xref ref-type="bibr" rid="CR35">35</xref>], by the use of serological and molecular methods as well as the Dienes test, proved that <italic>P. mirabilis</italic> strains isolated from feces and urine of patients were in fact the same spreading clone causing autoinfection and nosocomial infection. Wang et al. [<xref ref-type="bibr" rid="CR148">148</xref>] reported the case of food poisoning in a restaurant in Beijing, China, caused by <italic>P. mirabilis</italic>. The same clone, identified by genotyping and the Dienes method, was detected in the consumed food and in stools of consumers as well as the cook handler and the waiter who, due to the lack of hygiene, most probably had transported the bacteria to the meal. The fact that dirty hands may be an important step in feces-to-hand-to-mouth spread of <italic>Proteus</italic> spp. bacteria was also confirmed by other researchers. Smith et al. [<xref ref-type="bibr" rid="CR136">136</xref>] found <italic>P. vulgaris</italic> among the bacteria and yeasts isolated from roadside telephone receivers in Lagos, Nigeria. Padaruth and Biranjia-Hurdoyal [<xref ref-type="bibr" rid="CR110">110</xref>] detected <italic>Proteus</italic> spp. on hands of primary school pupils in Mauritius while Shojaei et al. [<xref ref-type="bibr" rid="CR132">132</xref>] on hands of food handlers in Iran (but simple washing resolved the problem). Also, Qadripur et al. [<xref ref-type="bibr" rid="CR119">119</xref>] found <italic>P. mirabilis</italic> to colonize hand skin between nail plate and nail fold in motor mechanics.</p><p>Peerbooms et al. [<xref ref-type="bibr" rid="CR113">113</xref>] compared <italic>P. mirabilis</italic> strains isolated from urine and feces, and all the isolates seemed to display similar virulence potential, which confirmed that the strains attacking the urinary tract may come from the intestinal reservoir. Also, Senior and Leslie [<xref ref-type="bibr" rid="CR130">130</xref>] concluded that frequent isolation of <italic>P. mirabilis</italic> from feces and rare occurrence of <italic>P. vulgaris</italic> in the intestines of healthy individuals and those suffering from gastroenteritis may explain the fact that it is the first species and not the second one that is strongly connected with urinary tract infections.</p><p>The presence of <italic>P. mirabilis</italic> in the intestines may also be connected with obesity. Lecomte et al. [<xref ref-type="bibr" rid="CR74">74</xref>], conducting research on an animal model, have recently reported on the changes in gut microflora depending on diet. Studying the intestinal microbiota of rats fed a high-fat diet (43 or 51 % of fat), the authors noticed higher numbers of <italic>P. mirabilis</italic> as compared to the control group (12 % fat diet). Moreover, a significant positive correlation was found between the abundance of <italic>P. mirabilis</italic> (as well as <italic>Phascolarctobacterium</italic> and <italic>Veillonellaceae</italic>) and all ten analyzed metabolic parameters associated with obesity.</p></sec><sec id="Sec4"><title><italic>Proteus</italic> spp. in Animals—Adverse and Friendly</title><p>Not only rats but also many wild and domestic animals (mammals, birds, reptiles, amphibians, insects, and “seafood”) are the hosts of <italic>Proteus</italic> spp. bacteria. The relation of the bacteria to their host organism is sometimes not determined; in some cases, it may be symbiotic or change from neutral/commensal to parasitic (Table <xref rid="Tab3" ref-type="table">3</xref>). The microorganisms are an element of animal pathogenic or physiological microflora, especially in the intestines—a reservoir of the bacteria.<table-wrap id="Tab3"><label>Table 3</label><caption><p>Different kinds of relationship between <italic>Proteus</italic> spp. and other organisms (details in the text): “+” positive (beneficial), “?” neutral/commensal/not determined, “−” negative (antagonistic, pathogenic)</p></caption><table frame="hsides" rules="groups"><thead><tr><th>organisms</th><th><italic>Proteus</italic> sp.</th><th><italic>P. mirabilis</italic></th><th><italic>P. vulgaris</italic> group</th><th><italic>P. penneri</italic></th><th>selected references</th></tr></thead><tbody><tr><td>Humans</td><td></td><td>? / −</td><td>? / −</td><td>? / −</td><td>8, 36, 81, 103, 124, 125, 148</td></tr><tr><td>Gorillas</td><td></td><td>?</td><td>?</td><td></td><td>15</td></tr><tr><td>Dogs</td><td>−</td><td>? / −</td><td>?</td><td>?</td><td>38, 44, 69, 99, 144</td></tr><tr><td>Cats, feral cats</td><td>−</td><td>−</td><td></td><td></td><td>54, 69, 99</td></tr><tr><td>Pigs</td><td></td><td>?</td><td>?</td><td></td><td>68, 75, 147</td></tr><tr><td>Horses</td><td>? / −</td><td></td><td></td><td></td><td>84, 152</td></tr><tr><td>Donkeys</td><td>−</td><td></td><td></td><td></td><td>83</td></tr><tr><td>Cow, cattle, calf</td><td></td><td>?</td><td>? / −</td><td>?</td><td>2, 56, 76, 123, 138</td></tr><tr><td>Raccoon dog</td><td></td><td></td><td>?</td><td></td><td>66</td></tr><tr><td>Flying fox</td><td></td><td>+</td><td>+</td><td></td><td>6</td></tr><tr><td>Rats</td><td></td><td>?</td><td></td><td></td><td>73</td></tr><tr><td>Birds, poultry</td><td>− (eggs)</td><td>?/−</td><td>? / −</td><td>? / −</td><td>9, 43, 46, 61, 62, 68, 71, 123, 154, 155, 161</td></tr><tr><td>Snakes</td><td></td><td>?</td><td>?</td><td>?</td><td>16, 53, 131</td></tr><tr><td>Alligator</td><td>−</td><td></td><td></td><td></td><td>101</td></tr><tr><td>Turtles</td><td>−</td><td>?</td><td>? / −</td><td>? / −</td><td>5, 10, 42, 53, 102, 108, 127</td></tr><tr><td>Amphibians</td><td></td><td></td><td>?</td><td></td><td>53</td></tr><tr><td>Fishes</td><td>+ / ?</td><td>+</td><td>+ / ? /−</td><td>+</td><td>17, 66, 70, 97, 107, 141</td></tr><tr><td>Oysters</td><td></td><td>?</td><td></td><td></td><td>39</td></tr><tr><td>Shrimps</td><td>+ / ?</td><td>+ / ?</td><td>+ / ?</td><td>+ / ? / −</td><td>20, 82, 97, 98</td></tr><tr><td>Lobsters</td><td>+</td><td>+</td><td>+</td><td>+</td><td>97</td></tr><tr><td>Blue crab</td><td></td><td></td><td></td><td>?</td><td>109</td></tr><tr><td>Sponges</td><td></td><td>+/?</td><td>?</td><td></td><td>50, 64</td></tr><tr><td>Millipede</td><td></td><td>+</td><td></td><td></td><td>4</td></tr><tr><td>Lepidopteran</td><td></td><td></td><td>−</td><td></td><td>85</td></tr><tr><td>Cockroaches</td><td></td><td>?</td><td>?</td><td></td><td>142, 145, 149</td></tr><tr><td>Honey bees</td><td>?</td><td></td><td></td><td></td><td>137</td></tr><tr><td>Flies</td><td>?</td><td>? / +</td><td>?</td><td></td><td>18, 51, 79, 80, 85, 87, 94, 134, 144, 150</td></tr><tr><td>Mites</td><td></td><td></td><td>+</td><td></td><td>2</td></tr><tr><td>Nematodes</td><td></td><td></td><td></td><td>−</td><td>76</td></tr><tr><td>Leguminous plants</td><td></td><td></td><td>+</td><td></td><td>12, 14, 120</td></tr><tr><td>Wild grass</td><td></td><td>+</td><td></td><td></td><td>121</td></tr><tr><td>Tea</td><td></td><td></td><td>+</td><td></td><td>12</td></tr><tr><td>Cabbage</td><td></td><td></td><td>+</td><td></td><td>156</td></tr><tr><td>Maize</td><td></td><td>+</td><td></td><td></td><td>60</td></tr><tr><td>Mould fungi</td><td>−</td><td></td><td>−</td><td></td><td>11, 12</td></tr><tr><td><italic>C. albicans</italic></td><td></td><td>−</td><td></td><td></td><td>50</td></tr><tr><td><italic>B. bacteriovorus</italic></td><td></td><td></td><td></td><td>−</td><td>20</td></tr></tbody></table></table-wrap></p><p><italic>P. mirabilis</italic> and <italic>P. vulgaris</italic> were found in fecal samples of western lowland gorillas (<italic>Gorilla gorilla gorilla</italic>), collected at two locations in south-central Cameroon, proving to inhabit the intestines of these great wild apes [<xref ref-type="bibr" rid="CR15">15</xref>]. Like in humans, the presence of <italic>Proteus</italic> spp. in animal intestines may pose a threat of autoinfection and cross-infection. The example of such autoinfection was described by Gaastra et al. [<xref ref-type="bibr" rid="CR44">44</xref>], who in the Netherlands isolated <italic>P. mirabilis</italic> strains from feces and urine of dogs suffering from recurrent urinary tract infections. It is probable that the intestine was a reservoir of the bacteria infecting the urinary tract of the dogs, because <italic>P. mirabilis</italic> strains were not isolated from feces of healthy controls. Also, Kroemer et al. [<xref ref-type="bibr" rid="CR69">69</xref>] reported <italic>P. mirabilis</italic> strains as a reason for urinary tract infections in dogs and cats in European countries. Normand et al. [<xref ref-type="bibr" rid="CR99">99</xref>] indicated <italic>Proteus</italic> spp. isolated from different materials (mostly feces, urine, skin swabs, upper respiratory tracks) as an important cause of illness in dogs and cats examined in Glasgow, UK. Moreover, 26 % of the strains were identified as multiple drug resistant. <italic>P. mirabilis</italic> was isolated from the rectum, the vagina, the mouth, the nose, and wound/abscess of feral cats analyzed in Grenada, West Indies [<xref ref-type="bibr" rid="CR54">54</xref>]. However, all the isolates were sensitive to most of the used antibiotics, so it was concluded that feral cats did not pose a risk to humans or other cats. Kitamikado and Lee [<xref ref-type="bibr" rid="CR66">66</xref>] isolated from feces of raccoon dog <italic>Nyctereutes procyonoides</italic>, a <italic>P. vulgaris</italic> strain producing chondroitinase, which may be regarded as one of the virulence factors produced by the microorganism because chondroitin sulfate is distributed in animal connective tissues.</p><p>On the other hand, there was no connection found between <italic>Proteus</italic> spp. and ulcerative keratitis [<xref ref-type="bibr" rid="CR146">146</xref>] or transmissible venereal tumor [<xref ref-type="bibr" rid="CR38">38</xref>] in dogs, as <italic>P. penneri</italic> and <italic>P. vulgaris</italic> strains were isolated from the eyes of healthy dogs in Beijing, China, and, respectively, <italic>P. mirabilis</italic> from the vagina of a healthy dog in Nigeria, but not from sick animals.</p><p><italic>Proteus</italic> spp. bacteria may also be the members of natural microflora of the esophagus [<xref ref-type="bibr" rid="CR84">84</xref>] and the skin of horses, although they were also isolated from wounds [<xref ref-type="bibr" rid="CR152">152</xref>]. However, the wound isolates displayed strong adherence and significantly stronger attachment than skin isolates proving enhanced virulence of pathogenic strains, as compared to normal skin isolates. The bacteria are virulent also to donkeys causing urinary tract infections. They were found to account for 6.7 % of donkey uropathogens isolated in Ethiopia, among which <italic>Streptococcus</italic> spp. (43.3 % isolates) and <italic>E. coli</italic> (20 %) were dominating [<xref ref-type="bibr" rid="CR83">83</xref>].</p><p><italic>P. mirabilis</italic> and <italic>P. vulgaris</italic> were also detected as the elements of the microbial community in pigs. Lowe et al. [<xref ref-type="bibr" rid="CR75">75</xref>] revealed that the family <italic>Enterobacteriaceae</italic> was a minor but significant component of pig tonsil microflora in which <italic>P. mirabilis</italic> or <italic>P. vulgaris</italic> clones dominated. Wang et al<italic>.</italic> [<xref ref-type="bibr" rid="CR147">147</xref>] reported a <italic>P. vulgaris</italic> strain isolated from nasal swab of a pig from a food producing animal farm (sic!) that was carrying a chromosomally located staphylococcal multiresistance <italic>cfr</italic> gene encoding the resistance to linezolid, but also to other chemically unrelated classes of antimicrobial agents. The gene was for the first time reported in a naturally occurring Gram-negative bacterium. Still Kobashi et al. [<xref ref-type="bibr" rid="CR68">68</xref>] isolated <italic>P. mirabilis</italic> strains from pig feces detecting the efflux genes responsible for their resistance to tetracycline (<italic>tetH</italic> and <italic>tetJ</italic>).</p><p>All <italic>Proteus</italic> species were detected in the cow. Hawkey et al. [<xref ref-type="bibr" rid="CR56">56</xref>] revealed that <italic>P. vulgaris</italic> (including the strains currently numbered among genomospecies) as well as <italic>P. mirabilis</italic> species were, respectively, the first and the third species among the tribe <italic>Proteeae</italic> most commonly isolated from beddings contaminated with feces and urine in two calf farms in South West England. The authors concluded that the high similarity of the O-serotype profile of isolated strains (e.g., serotypes O23 and O30) to those reported for human infections (Table <xref rid="Tab2" ref-type="table">2</xref>) suggests that food animals may be a source of <italic>Proteeae</italic> strains carried in human gut. Lu et al. [<xref ref-type="bibr" rid="CR76">76</xref>] reported on the isolation from a cow dung in China of <italic>P. penneri</italic> strains displaying strong nematicidal activity. <italic>P. vulgaris</italic> seems to belong to normal skin microflora of cattle, but the involvement of these bacteria in the damage to tissues around the skin lesions caused by <italic>Demodex bovis</italic> mite and their synergistic influence was also revealed [<xref ref-type="bibr" rid="CR2">2</xref>]. The symbiosis between the parasites relies on the fact that the mite introducing the bacteria into the skin on the exoskeleton or in the gut receives suitable microclimate for the establishment and replication due to many virulence factors and enzymes produced by the cooperating microorganisms.</p><p>Rogers [<xref ref-type="bibr" rid="CR123">123</xref>] suggested a possibility of the transmission of potentially pathogenic bacteria, including <italic>Proteus</italic> spp., between wild birds and cattle. The author stated the presence of <italic>P. vulgaris</italic> in feces of 13 % dairy cattle in five studied farms, and in fecal and cloacal samples from 7.8 % analyzed birds (sparrows, blackbirds, cowbirds, but not starlings).</p><p>Other authors also emphasized the role of wild birds in the transmission and spread of pathogenic bacteria to domestic poultry, cattle, or humans, resulting in the change of their status from bird fecal microflora members to the etiological agent of pathogenesis. Yong et al. [<xref ref-type="bibr" rid="CR155">155</xref>] found <italic>P. mirabilis</italic> to be prevalent in feces of large-billed crows (<italic>Corvus</italic> spp.) inhabiting the surroundings of a minimarket in Bangsar, Malaysia, and becoming a health hazard due to their large numbers. However, no bacteria (with the exception of <italic>Klebsiella</italic> spp.) were present in the air samples from the market place. Winsor et al. [<xref ref-type="bibr" rid="CR154">154</xref>] conducted studies on fecal microflora of apparently healthy wild turkey vultures (<italic>Cathartes aura</italic>) in Texas, USA, because the diet of these birds, which are carrion-feeding animals, must include animals that have died of infectious diseases. The content of the studied bird intestines was dominated by <italic>E. coli</italic> but, in fact, <italic>P. mirabilis</italic> was the second predominant species detected in 50 % birds and <italic>P. vulgaris</italic> was isolated from one bird. Jahantigh [<xref ref-type="bibr" rid="CR61">61</xref>, <xref ref-type="bibr" rid="CR62">62</xref>] stated that <italic>Proteus</italic> spp. strains in 2010 accounted for 5 % and in 2012 for 12.5 % isolates from eggs of the ostrich (<italic>Struthio camelus</italic>). The authors indicated fecal contamination that may lead to the penetration of the bacteria into the egg interior and the infection which may be a reason for a relatively high ratio of embryonic mortality in ostrich eggs in Iran. Awad-Alla et al. [<xref ref-type="bibr" rid="CR9">9</xref>] suggested a possible role of white ibises (<italic>Nipponia nippon</italic>) in Egypt in the transmission of some pathogens to poultry as in the internal organs of apparently healthy birds they found several strains classified as <italic>P. mirabilis</italic> (although the indicated ability of indole production suggests that the strains should be identified as <italic>P. vulgaris</italic>; see Table <xref rid="Tab1" ref-type="table">1</xref>). Next, Foti et al. [<xref ref-type="bibr" rid="CR43">43</xref>] conducted studies on the health status of birds belonging to several orders migrating to Africa through the Ustica Island (Italy). From fecal swabs and internal organs of birds found dead, they isolated only one <italic>P. mirabilis</italic> strain, so the probability of dissemination of these bacteria was very low. Kwiecińska-Piróg et al. [<xref ref-type="bibr" rid="CR71">71</xref>] revealed that <italic>P. mirabilis</italic> naturally occurring in the crop and the cloaca of white stork (<italic>Ciconia ciconia</italic>) healthy nestlings in Poland were more susceptible to antibiotics than clinical strains isolated from human beings and no ESBL production was detected.</p><p>The above data indicate that the presence of <italic>Proteus</italic> spp. in birds does not pose a real risk of dissemination; moreover, <italic>Proteus</italic> spp. bacteria seem to be a member of normal poultry microflora. Among the bacteria inhabiting the beak cavity and the cloaca of reproductive goose flocks (190–800 birds) from 17 farms in Poland, <italic>Proteus</italic> spp. colonized approximately 10–25 % of birds [<xref ref-type="bibr" rid="CR161">161</xref>], while <italic>E. coli</italic>, <italic>Enterococcus</italic> spp., and <italic>Streptococcus</italic> spp. were found in approximately 60–70 % of birds and coagulase-negative <italic>Staphylococcus</italic> was isolated from 80–90 % birds, independently of the sampling site. Other bacteria were isolated sporadically. Also, Kobashi et al. [<xref ref-type="bibr" rid="CR68">68</xref>] isolated <italic>P. mirabilis</italic> and <italic>Proteus</italic> sp. strains from poultry feces, detecting the <italic>tetM</italic> gene, encoding their resistance to tetracycline. However, Giacopello et al. [<xref ref-type="bibr" rid="CR46">46</xref>] recognized antibiotic-resistant <italic>P. mirabilis</italic>, <italic>P. vulgaris</italic>, and <italic>P. penneri</italic> present in feces of sick domestic canaries as pathogenic microflora.</p><p><italic>Proteus</italic> spp. colonize also amphibians and reptiles, e.g., <italic>P. vulgaris</italic> is reported as a common inhabitant both in the oral cavity and in the cloaca of water amphibians (<italic>Lissotriton vulgaris</italic> newts and <italic>Pelophylax ridibundus</italic> frogs) and reptiles (<italic>Mauremys rivulata</italic> turtles and <italic>Natrix natrix</italic> grass snakes) inhabiting the Kavak Delta, Turkey [<xref ref-type="bibr" rid="CR53">53</xref>]. In the oral bacterial flora of Chinese cobra, <italic>Naja atra</italic>, and bamboo pit vipers, <italic>Thimeresurus albolabris</italic>, two snake species common in Hong Kong [<xref ref-type="bibr" rid="CR131">131</xref>], <italic>P. penneri</italic>, <italic>P. vulgaris</italic>, and <italic>P. mirabilis</italic> strains were isolated among many other potentially pathogenic bacteria. Blaylock [<xref ref-type="bibr" rid="CR16">16</xref>] reported on the common isolation of <italic>Proteus</italic> sp., <italic>P. mirabilis</italic>, and <italic>P. vulgaris</italic> from oral swabs of four different house snake species from southern Africa. There is also a report on pathogenic <italic>Proteus</italic> sp. as a cause (together with <italic>Morganella morganii</italic>) of the septicemia and death of a captive alligator held in the Savannah River Ecology Laboratory in Aiken, SC, USA [<xref ref-type="bibr" rid="CR101">101</xref>].</p><p>There are several reports available concerning the presence of <italic>Proteus</italic> spp. bacteria in water turtles, sometimes connected with illness. They were the fourth genus most frequently isolated from lesions of sea turtles from the Canary Islands, Spain, and were considered as one of the causes of their diseases and mortality [<xref ref-type="bibr" rid="CR108">108</xref>]. Al-Bahry et al. [<xref ref-type="bibr" rid="CR5">5</xref>] interpreted the presence of <italic>Proteus</italic> spp. and <italic>P. vulgaris</italic> (resistant to ampicillin, streptomycin, and tetracycline) in oviductal fluids of nesting sea green turtles (<italic>Chelonia mydas</italic>) as an indicator of pollution in the surrounding areas between the Gulf of Oman and the Arabian Sea (see the next paragraph). In contrast, in nesting green turtles from Costa Rica, <italic>P. mirabilis</italic> and <italic>P. vulgaris</italic> bacteria were recognized as a non-pathogenic constituent of microflora. They were isolated from nasal and cloacal swabs from apparently healthy turtle females with no signs of disease. There was no correlation observed between the turtles and seawater bacteria composition, so it was suggested that <italic>Proteus</italic> bacteria should be treated as the physiological microflora of green turtles [<xref ref-type="bibr" rid="CR127">127</xref>]. <italic>P. mirabilis</italic> was also commonly found as inhabiting the cloaca of European pond turtles (<italic>Emys orbicularis</italic>), especially captive ones, from Poland [<xref ref-type="bibr" rid="CR102">102</xref>]. <italic>P. vulgaris</italic> was the predominant species, and some <italic>P. mirabilis</italic> strains were also identified in cloacal and oral swabs of loggerhead sea turtles (<italic>Caretta caretta</italic>) inhabiting the Sicilian Channel, the South Tyrrhenian Sea, and the Ionian Sea [<xref ref-type="bibr" rid="CR42">42</xref>]. The loggerhead turtle is included in the Red List of the world conservation union, and the microbial contamination of the turtle eggs is suspected to play a role in embryonic death and a low loggerhead hatch success rate in Georgia, USA. Indeed, among other Gram-negative isolates from unhatched eggs of the turtle on Jekyll Island, Georgia, <italic>P. penneri</italic> and <italic>P. vulgaris</italic> strains were identified [<xref ref-type="bibr" rid="CR10">10</xref>].</p><p>Although <italic>Proteus</italic> spp. bacteria are commonly known as opportunistic pathogens, there can be found interesting examples of positive relations between the microorganisms and the host animal (Table <xref rid="Tab3" ref-type="table">3</xref>). <italic>P. mirabilis</italic> and <italic>P. vulgaris</italic> strains isolated from the intestine of the Indian flying fox (<italic>Pteropus giganteus</italic>) were recognized as the members of symbiotic physiological microflora of this big fruit bat [<xref ref-type="bibr" rid="CR6">6</xref>]. Although this is unusual for the two species (Table <xref rid="Tab4" ref-type="table">4</xref>), the isolates were able to produce cellulolytic and xylanolytic enzymes just as three other isolated species, <italic>Citrobacter freundii</italic>, <italic>Serratia liquefaciens</italic>, and <italic>Klebsiella oxytoca</italic>, and contrary to the other six gut isolates unable to digest cellulose. Fruits and leaves, which are the animal’s main food, are built of up to 50 % of cellulose, hemicellulose (xylan), lignocellulose, and pectin cellulose, and because mammals do not possess proper enzymes to degrade the polymers, the symbiotic enterobacteria play an essential role in their nourishment and digestion. Another example of a cellulolytic and xylanolytic <italic>P. mirabilis</italic> strain isolated as a gut symbiont of millipede (<italic>Xenobolus carnifex</italic>) was reported by Alagesan et al. [<xref ref-type="bibr" rid="CR4">4</xref>].<table-wrap id="Tab4"><label>Table 4</label><caption><p>Unusual physiological features displayed by <italic>Proteus</italic> spp. strains isolated from different habitats (details in the text)</p></caption><table frame="hsides" rules="groups"><thead><tr><th>Feature</th><th><italic>Proteus</italic> sp.</th><th><italic>P. mirabilis</italic></th><th><italic>P. vulgaris</italic></th><th><italic>P. hauseri</italic></th></tr></thead><tbody><tr><td>Heterotrophic nitrification</td><td></td><td>Coastal seawater</td><td></td><td></td></tr><tr><td>Cellulose digestion</td><td></td><td>Flying fox, millipede</td><td>Flying fox</td><td></td></tr><tr><td>Lipase production/hydrocarbons utilization (including aromatic ones)</td><td>Contaminated soil; waste sludge</td><td>Contaminated soil</td><td>Contaminated soil; contaminated fish</td><td></td></tr><tr><td>Phenol utilization</td><td></td><td>Contaminated soil</td><td></td><td></td></tr><tr><td>Methyl tert-butyl ether (MTBE) degradation</td><td></td><td>Contaminated soil</td><td></td><td></td></tr><tr><td>ɛ-Caprolactam utilization</td><td></td><td>Contaminated soil</td><td></td><td></td></tr><tr><td>Hexachlorocyclohexane (HCH) pesticide utilization</td><td>Contaminated soil</td><td></td><td></td><td></td></tr><tr><td>Phorate pesticide utilization</td><td>Contaminated soil</td><td></td><td></td><td></td></tr><tr><td>Chlorpyrifos, methyl parathion, and p-nitrophenol pesticides degradation</td><td>Contaminated soil (in consortium)</td><td>Contaminated soil (in consortium)</td><td></td><td></td></tr><tr><td>DDT reduction</td><td></td><td></td><td>Mouse</td><td></td></tr><tr><td>Azo dyes decolorizing</td><td>Waste site</td><td>Contaminated soil; wastewater sludge</td><td></td><td>Hot spring</td></tr><tr><td>Phosphate solubilization</td><td>Phorate contaminated soil</td><td>Wild grass rhizosphere</td><td></td><td></td></tr><tr><td>Copper tolerance</td><td></td><td>Wild grass rhizosphere; wastewater</td><td>Soil</td><td>Hot spring</td></tr><tr><td>Chromium,cobalt, cadmium, zinc,mercury, nickel, lead, arsenic tolerance</td><td></td><td>Wild grass rhizosphere; wastewater; contaminated soil</td><td></td><td></td></tr><tr><td>Silver tolerance</td><td></td><td>Wastewater</td><td></td><td></td></tr><tr><td>Chromate tolerance</td><td>Contaminated seawater</td><td></td><td></td><td></td></tr><tr><td>Thermotolerance</td><td></td><td></td><td></td><td>Hot spring</td></tr><tr><td>Halotolerance</td><td>Salt lake</td><td>Oysters</td><td>Halophyte glasswort rhizosphere</td><td></td></tr><tr><td>Acidotolerance</td><td>Soil contaminated by hydrocarbons</td><td></td><td>Acidic soil</td><td>Hot spring</td></tr></tbody></table></table-wrap></p><p>Also, a symbiotic role has been suggested for <italic>P. mirabilis</italic> and <italic>P. vulgaris</italic> isolated from hematophagous sand fly <italic>Phlebotomus papatasi</italic> being a vector of <italic>Leishmania</italic> parasite, as the bacteria were the most prevalent in larvae, pupae, and mature male and female insects gut [<xref ref-type="bibr" rid="CR80">80</xref>]. Another very interesting hypothesis indicating a close relationship between <italic>P. mirabilis</italic> and its blowfly host <italic>Lucilia sericata</italic> was formed by Ma et al. [<xref ref-type="bibr" rid="CR79">79</xref>]. These proteolytic microorganisms are able to produce volatile components, for example, putrescine (from ornithine) and ammonia (see Table <xref rid="Tab1" ref-type="table">1</xref>), important for their swarming ability and, at the same time, attracting flies to the carcass. The authors stated that putrescine, which is an extracellular signal required for the swarming phenomenon and used by <italic>P. mirabilis</italic> in <italic>quorum sensing</italic> [<xref ref-type="bibr" rid="CR89">89</xref>], may be an interkingdom signal sensed by both the insects and the bacteria. The same role was suggested for ammonia. Both compounds as well as four other attractants (NaOH, KOH, phenol, and lactic acid) restored the swarming motility in different swarming-deficient mutants of the <italic>P. mirabilis</italic> strain isolated from maggot salivary glands where they dominated, so the researchers linked fly attraction with <italic>Proteus</italic> swarming. The bacteria were detected also in adult <italic>L. sericata</italic> flies and in <italic>Lucilia cuprina</italic> sister species [<xref ref-type="bibr" rid="CR134">134</xref>]. The symbiosis between blowflies and <italic>Proteus</italic> bacteria is also indicated by the fact that <italic>P. mirabilis</italic> biofilm, contrary to biofilms constructed by <italic>Staphylococcus aureus</italic> and <italic>Enterobacter cloacae</italic>, is not disrupted or is even stimulated by <italic>L. sericata</italic> maggots used in the debridement therapy. Simultaneously, <italic>P. mirabilis</italic> is antagonistic to some bacteria eliminated by maggots from wounds, protecting the larvae from harmful microorganisms [<xref ref-type="bibr" rid="CR18">18</xref>]. Complete sterility of <italic>L. cuprina</italic> maggots for wound therapy was achieved in all cases except for <italic>P. mirabilis</italic> [<xref ref-type="bibr" rid="CR87">87</xref>]. Additionally, Wei et al. [<xref ref-type="bibr" rid="CR150">150</xref>] revealed that both sensitive and antibiotic-resistant <italic>P. mirabilis</italic> strains could persist for several days among the gut microflora of the green bottle fly (<italic>L. sericata</italic>) or the housefly (<italic>Musca domestica</italic> L.) when introduced by feeding. It has been speculated that the mechanisms stimulated by the fly host may contribute to the maintaining of antibiotic-resistant strains in particular, and in that way, their transmission is imminent. It was also suggested [<xref ref-type="bibr" rid="CR144">144</xref>] that flies, as the vectors of bacteria to raw meat devoted to dog breeding, were responsible for a high percentage of morbidity and mortality due to intestinal infections among pups in greyhound dog kennels in Kansas, USA. A high percentage of bacterial contamination among blowflies (different species) and domestic flies (<italic>M. domestica</italic>), stable flies (<italic>Stomoxys calcitrans</italic> L.), flesh flies, and others was observed, while <italic>Proteus</italic> spp. were proved to be the most common bacteria among Gram-negative and lactose-negative ones isolated from flies, followed by <italic>Providencia</italic> spp., <italic>Pseudomonas</italic> spp., and <italic>Salmonella</italic> spp. Nazni et al. [<xref ref-type="bibr" rid="CR94">94</xref>] identified <italic>Proteus</italic> as the second (after <italic>Enterobacter</italic>) dominating genus on the external body surface, while in the fly gut, <italic>Proteus</italic> spp. dominated among the bacteria isolated from the housefly (<italic>M. domestica</italic>) on a poultry farm in Malaysia. <italic>P. mirabilis</italic> with <italic>Providencia</italic> spp. was also prevalent in gut microflora of flies captured in different public places in India [<xref ref-type="bibr" rid="CR51">51</xref>].</p><p>Not only flies but also cockroaches are regarded as common vectors of different microorganisms, including <italic>P. mirabilis</italic> and <italic>P. vulgaris</italic> strains, carrying them on their bodies and posing a threat of their dissemination, food contamination, and spoiling as well as infection of humans. The bacteria were found in Nigerian cockroaches in Ekpoma, a village characterized by poor sanitary conditions [<xref ref-type="bibr" rid="CR142">142</xref>], and in Iranian brown-banded cockroaches collected in kitchens of Ahvaz houses [<xref ref-type="bibr" rid="CR145">145</xref>]. Wannigama et al. [<xref ref-type="bibr" rid="CR149">149</xref>] reported on the isolation of <italic>P. mirabilis</italic> from 8.9 % cockroaches found in households and food-handling establishments in Varanasi, India.</p><p><italic>P. vulgaris</italic> was isolated from tissues of an American fly <italic>Drosophila paulistorum</italic> [<xref ref-type="bibr" rid="CR85">85</xref>], although it was not determined if the microorganisms were parasitic, mutualistic, or symbiotic to their host. However, they displayed strong pathogenicity toward lepidopterans like <italic>Heliothis virescens</italic>. Other insects which may carry <italic>Proteus</italic> spp. bacteria in the intestines are bees [<xref ref-type="bibr" rid="CR137">137</xref>]. It is suggested that the source of the bacteria is pollen consumption and bees in the colony are infected one by one during food exchange. Honey pollution by <italic>Proteus</italic> spp. may pose a threat to consumers.</p><p>A similar situation may be observed in water animals, so called “seafood,” where the presence of <italic>Proteus</italic> spp. may result in food spoiling and poisoning, e.g., scombroid poisoning of fish meat as a result of histidine decarboxylation leading to a rise in the level of toxic histamine [<xref ref-type="bibr" rid="CR100">100</xref>]. A source of bacteria, including antibiotic-resistant ones, may be fecally contaminated water (see the next paragraph), because <italic>P. vulgaris</italic> and <italic>P. mirabilis</italic> rods were found as absorbed on body structures of the commercially important sponge <italic>Spongia officinalis</italic>, an animal inhabiting the Aegean Sea and feeding by the seawater filtration [<xref ref-type="bibr" rid="CR64">64</xref>]. Also, Graça et al. [<xref ref-type="bibr" rid="CR50">50</xref>] reported on the isolation of several <italic>Proteus</italic> sp. strains (closely related to <italic>P. mirabilis</italic>) from the marine sponge (<italic>Erylus deficiens</italic>) collected 150 km off the southwest coast of Portugal. The authors revealed that <italic>Proteus</italic> sp. strains (together with <italic>Pseudoalteromonas</italic> and <italic>Microbacterium</italic> spp. isolates) presented the strongest bioactivity against pathogenic bacteria and <italic>Candida albicans</italic>, thus protecting the host animal and assisting its survival, also due to the fact that the absorbed bacteria constitute 50–60 % of the sponge biomass.</p><p>However, the occurrence of these opportunistic human pathogens in oysters poses a health risk if the shellfish are consumed raw. Fernandez-Delgado et al. [<xref ref-type="bibr" rid="CR39">39</xref>] found halophilic (growth in saline concentrations from 3 to 8 %) <italic>P. mirabilis</italic> as prevailing in the bodies of two oyster species in Venezuela and resistant to several tested antibiotics (mainly tetracycline, ampicillin and penicillin, and cefoxitin and cefazolin). Also, Matyar et al. [<xref ref-type="bibr" rid="CR82">82</xref>] isolated several antibiotic-resistant <italic>P. vulgaris</italic> and <italic>P. penneri</italic> strains from the intestines of shrimps inhabiting the Iskenderun Bay, Turkey, which was most probably due to the Iskedrun Bay contamination by industrial and domestic wastes, including hospital ones. It is worth noting that <italic>Proteus</italic> spp. strains were absent from seawater and sediments, although high amounts of fecal coliforms indicated strong fecal contamination of the Bay. Nimrat et al. [<xref ref-type="bibr" rid="CR98">98</xref>] identified <italic>Proteus</italic> spp. and <italic>P. mirabilis</italic> among other bacteria detected in spermatophores from black tiger shrimps (<italic>Penaeus monodon</italic>) collected from the Andaman Sea, Thailand. Cao et al. [<xref ref-type="bibr" rid="CR20">20</xref>] recognized <italic>P. penneri</italic> as an agent causing red body disease of commercial white shrimps <italic>Penaeus vannamei</italic>, cultivated in Xiaoshan, Zheijang, China. Interestingly, the mortality of shrimps was successfully inhibited by the predatory activity of <italic>Bdellovibrio bacteriovorus</italic> against the <italic>P. penneri</italic> pathogen; thus, the authors propose this bacterial predator as a potential biocontrol agent. <italic>P. penneri</italic> strain inter alia was also detected on the body surface of the wild blue crab (<italic>Callinectes sapidus</italic>) in the Akyatan Lagoon (the south of the Mediterranean Sea) [<xref ref-type="bibr" rid="CR109">109</xref>].</p><p><italic>Proteus</italic> spp. rods are found in marine fishes. In Atlantic mackerel (<italic>Scomber scombrus</italic>), <italic>P. vulgaris</italic> and <italic>Proteus</italic> sp. were detected in gills, skin, and gut as the only members of the family <italic>Enterobacteriaceae</italic> [<xref ref-type="bibr" rid="CR141">141</xref>]. In <italic>Scomber japonicus</italic> mackerel (the intestine and the stomach) or in <italic>Limanda herzensteini</italic> flat fish (the gills), <italic>P. vulgaris</italic> was stated as producing a big yield of intracellular and extracellular chondroitinase, which may be directed against the host connective tissues, containing mucopolysaccharide chondroitin [<xref ref-type="bibr" rid="CR66">66</xref>]. Also, freshwater Nile tilapias (<italic>Oreochromis niloticus</italic>) from experimental freshwater aquaculture in Brazil [<xref ref-type="bibr" rid="CR17">17</xref>] and tilapias from Lake Victoria, Kenya [<xref ref-type="bibr" rid="CR107">107</xref>], were sporadically colonized by <italic>P. vulgaris</italic> or <italic>Proteus</italic> sp. Kumar et al. [<xref ref-type="bibr" rid="CR70">70</xref>] reported on <italic>P. hauseri</italic> as a causative agent of hemorrhage and mortality in a koi carp (<italic>Cyprinus carpio</italic>) farm in India. This is the first animal habitat reported for this poorly recognized species, while the sources of isolation of two previously described <italic>P. hauseri</italic> strains (one human) remain unknown [<xref ref-type="bibr" rid="CR104">104</xref>] and two other strains were isolated from human urine [<xref ref-type="bibr" rid="CR63">63</xref>].</p><p>The presence of <italic>Proteus</italic> spp. bacteria was also revealed to have a surprisingly positive influence on water animals. Many <italic>P. mirabilis</italic>, <italic>P. vulgaris</italic>, <italic>P. penneri</italic>, <italic>P.</italic> genomospecies 4, and unidentified <italic>Proteus</italic> sp. strains isolated from the intestines of black tiger shrimp, cobia marine fish, snubnose pompano marine fish, and ornate spiny lobster in Vietnam demonstrated probiotic properties linked to bacteriocin production and their antagonistic activity towards many pathogenic bacteria [<xref ref-type="bibr" rid="CR97">97</xref>].</p></sec><sec id="Sec5"><title><italic>Proteus</italic> as an Indicator of Fecal Pollution</title><p>The presence of <italic>Proteus</italic> spp. bacteria in water and soil may indicate the fecal pollution of the environments where these proteolytic bacteria are treated as allochthonic. Human and animal feces are probably an important source of these rods in natural environments. Water animals may absorb pollutant microorganisms from water. There is a potential risk of their spread in the marine food chain as well as dissemination during the food processing and transmission to humans after consumption. For instance, bacteria (in that number <italic>Proteus</italic> spp.) associated with sponges (<italic>S. officinalis</italic>), which are the main filter feeders in marine environment, were proposed to be treated as indicators of fecal contamination of marine ecosystems [<xref ref-type="bibr" rid="CR64">64</xref>]. Other marine animals that are reported to accumulate <italic>Proteus</italic> spp. from water environment are oysters [<xref ref-type="bibr" rid="CR39">39</xref>], loggerhead turtles (<italic>C. caretta</italic>) [<xref ref-type="bibr" rid="CR42">42</xref>], and green turtles (<italic>C. mydas</italic>) [<xref ref-type="bibr" rid="CR5">5</xref>], although Santoro et al. [<xref ref-type="bibr" rid="CR127">127</xref>] did not find the correlation between green turtle microflora and seawater microorganisms.</p><p>Also, antibiotic-resistant <italic>Proteus</italic> spp. strains may be released from the intestines which are a source of drug-resistance genes [<xref ref-type="bibr" rid="CR126">126</xref>]. Some authors [<xref ref-type="bibr" rid="CR5">5</xref>, <xref ref-type="bibr" rid="CR39">39</xref>, <xref ref-type="bibr" rid="CR82">82</xref>] emphasize the fact that marine environment seems to be a reservoir of genes responsible for the antibiotic resistance of polluting bacteria, as many antibiotic-resistant strains, including <italic>Proteus</italic> spp., are isolated from water and sea animals (see the previous paragraph). A good example is also the Jiaozhou Bay on the western coast of the Yellow Sea, China, which is highly contaminated due to intensive industrial development and urbanization. Effluents from hospitals and wastewater may be the sources of drug-resistant bacteria, allowing the resistance genes transfer to environmental microflora. Many bacterial strains resistant to tetracycline or chloramphenicol, including <italic>P. mirabilis</italic>, were isolated from the seawater by Dang et al<italic>.</italic> [<xref ref-type="bibr" rid="CR28">28</xref>, <xref ref-type="bibr" rid="CR29">29</xref>]. Also, in Cameroon studies of water samples collected for a period of 8 months from Douala Lagoon, contaminated by industrial and domestic wastes, resulted in the isolation of <italic>P. vulgaris</italic> strains among other fecal bacteria in each sample, which poses a serious health problem [<xref ref-type="bibr" rid="CR3">3</xref>].</p><p>The fact of <italic>Proteus</italic> spp. survival in marine environments indicates the ability of these microorganisms to adapt to higher salinity conditions, similarly to the strains from oysters, mentioned earlier. Indeed, several halotolerant <italic>Proteus</italic> spp. strains were detected in water samples from El Golea Salt Lake, Algerian Sahara, proving that domestic wastes from the El-Goela oasis could be a source of the fecal microflora surviving in these conditions [<xref ref-type="bibr" rid="CR52">52</xref>].</p><p><italic>Proteus</italic> spp. can also be found in freshwater, as an indicator of its contamination by feces, even in unexpected habitats. Microbiological investigation of water and sediments from the Vrelo Cave, the Republic of Macedonia [<xref ref-type="bibr" rid="CR33">33</xref>], revealed mostly the presence of <italic>Bacillus</italic> spp. strains (83 %), but, additionally, allochthonic strains were detected, including <italic>P. penneri</italic>, in a water sample taken from a place located 400 m from the cave entrance and 100 m deep. Moreover, although physical, chemical, and biochemical parameters indicated a high water quality, big numbers of total and fecal coliform bacteria were observed both in water and in sediment samples, suggesting their contamination from an animal source.</p><p>The detection of bacteria belonging to the genus <italic>Proteus</italic> in drinking water disqualifies its suitability for consumption due to its fecal pollution, which would threaten with waterborne infections. The problem occurs in India. <italic>P. vulgaris</italic> was claimed to be the main microbial pollutant of drinking water in Rajasthan [<xref ref-type="bibr" rid="CR140">140</xref>]. Then, in bore well waters in Mysore City, <italic>P. mirabilis</italic> and <italic>P. vulgaris</italic> strains dominated over the other H<sub>2</sub>S-producing strains (considered as associated to fecal coliforms in drinking water) [<xref ref-type="bibr" rid="CR93">93</xref>]. Poonia et al<italic>.</italic> [<xref ref-type="bibr" rid="CR117">117</xref>] reported on the alarming presence of multidrug resistant <italic>P. mirabilis</italic> and <italic>P. vulgaris</italic> strains among other bacteria in drinking water from springs and streams in the rural areas of Sikkim. Also, in Nigeria, <italic>Proteus</italic> spp. bacteria were detected in two of five studied well waters, treated as a source of drinking water [<xref ref-type="bibr" rid="CR1">1</xref>].</p><p><italic>P. mirabilis</italic>, <italic>P. vulgaris</italic>, and <italic>P. penneri</italic> strains, in addition to other members of <italic>Enterobacteriaceae</italic>, were recognized as bacteria connected with an anthropic influence, indicating the fecal contamination of rice field water from irrigation channels and rice field plots in Rio Grande do Sul, Brazil [<xref ref-type="bibr" rid="CR122">122</xref>].</p><p>Also, in soil, the presence of <italic>Proteus</italic> spp. bacteria is regarded as the evidence for its fecal contamination. Srinivasan et al. [<xref ref-type="bibr" rid="CR138">138</xref>] reported on the isolation of <italic>P. mirabilis</italic> strains from the soil samples from a dairy farm area that was regularly treated with cow manure, but not from the control forest soil samples with no history of agriculture. Trawińska et al<italic>.</italic> [<xref ref-type="bibr" rid="CR143">143</xref>] detected both <italic>Proteus</italic> spp. and <italic>E. coli</italic> strains in soil samples, collected near or 300 m from the reproductive layer farm in Poland, although the grounds were not treated with manure or exploited. Thus, it was suggested that the bacteria associated with fecal contamination of soil may have come from other animals, because the soil samples also contained <italic>Toxocara</italic> spp. eggs, which are not found in birds.</p></sec><sec id="Sec6"><title><italic>Proteus</italic> in Bioremediation and Plant Growth Promotion</title><p><italic>Proteus</italic> spp. bacteria, as an element of intestinal microflora of humans and animals, are often treated as zymogens in soil or water. In fact, these proteolytic microorganisms come to these environments with feces or waste, and after digestion of approachable organic matter, they decay due to the lack of nutrients.</p><p>However, these microorganisms are also found in such habitats as autochthones, well adapted to the environmental conditions, exhibiting unusual and exceptional metabolic features (Table <xref rid="Tab4" ref-type="table">4</xref>), although this aspect of the genus <italic>Proteus</italic> lifestyle is less known. An interesting example is a <italic>P. mirabilis</italic> strain isolated from coastal seawater in China, which was characterized as a heterotrophic nitrifier [<xref ref-type="bibr" rid="CR158">158</xref>]. The strain effectively removed ammonia (NH<sub>4</sub><sup>+</sup>) ions by oxidation. Moreover, only trace amounts of NO<sub>2</sub><sup>−</sup> and NO<sub>3</sub><sup>−</sup> were detectable after cultivation as the ions were simultaneously reduced by the bacterium to gaseous nitrogen (N<sub>2</sub>) in the denitrification processes. The processes and the cell growth were inhibited in the absence of any organic source of carbon. The strain is suggested to be used for toxic NH<sub>4</sub><sup>+</sup>-N removal, although its activity in oligotrophic water was limited probably due to the lack of carbon sources. Similar metabolic activity was displayed by the <italic>Proteus</italic> sp. strain related to <italic>P. mirabilis</italic>, isolated from effluents from a fish processing plant in India [<xref ref-type="bibr" rid="CR86">86</xref>]. Simultaneous aerobic nitrification and denitrification leading to the efficient removal of nitrogen by this heterotrophic bacterium are suggested to be applied in fish waste treatment.</p><p><italic>Proteus</italic> spp. bacteria, though well known as opportunistic pathogens, in natural environments show more positive aspects of their existence. They may play a role of effective and specialized plant-growth-promoting rhizobacteria (PGRP) or bioremediators of hydrocarbons, pesticides, herbicides, aromatic compounds, azo dyes, and heavy metals in contaminated environments.</p><p>Lipase production is not typical of all <italic>Proteus</italic> species (Table <xref rid="Tab1" ref-type="table">1</xref>), but the rods in natural environments are able to effectively degrade hydrocarbons, including oils, and to remove these hazardous substances efficiently and inexpensively. Kim et al<italic>.</italic> [<xref ref-type="bibr" rid="CR65">65</xref>] reported on a <italic>P. vulgaris</italic> strain producing extracellular alkaline lipase isolated from soil samples collected near a sewage disposal plant in South Korea. The lipase was stable from pH 5 to 11 and had a maximum activity at pH 10. Lu et al<italic>.</italic> [<xref ref-type="bibr" rid="CR77">77</xref>] isolated from soil in China a <italic>P. vulgaris</italic> strain which produced alkaline non-position-specific lipase, whereas Whangsuk et al<italic>.</italic> [<xref ref-type="bibr" rid="CR153">153</xref>] found in a waste-sludge from beer factory in Taiwan a <italic>Proteus</italic> sp. strain actively giving off organic-solvent-tolerant lipase named LipA, which effectively conversed palm oil into biodiesel.</p><p>The first report on a <italic>Proteus</italic> sp. strain which could be useful as a sole degrader of oil hydrocarbons in soil was presented by Hernandez-Rivera et al<italic>.</italic> [<xref ref-type="bibr" rid="CR57">57</xref>]. The strain may be presumed to belong to <italic>P. vulgaris</italic> group due to indole production and maltose fermentation abilities observed by the authors (see Table <xref rid="Tab1" ref-type="table">1</xref>). It was found in tropical soil containing total petroleum hydrocarbons (TPHs) in the Tabasco region, Mexico, highly contaminated by oil spills during 20 years of pollution and was able to remove the superficial hydrocarbon layer (the only carbon source) in the culture medium forming a stable emulsion, most probably due to the production of biosurfactants by the strain itself. The results were better than in the medium containing urea (actively utilized by the bacteria; see Table <xref rid="Tab1" ref-type="table">1</xref>). Then, Ibrahim et al<italic>.</italic> [<xref ref-type="bibr" rid="CR58">58</xref>] studying soil samples collected from the rhizosphere of legumes planted on crude-oil-contaminated soil in Kaduna, Nigeria, found <italic>P. mirabilis</italic> and <italic>P. vulgaris</italic> strains as belonging to the most active crude oil degraders among the several isolated species, although not displaying biosurfactant production. Earlier, another hydrocarbon degrading <italic>P. vulgaris</italic> strain had been isolated from newly killed fish samples that were collected near the point of spill in the Niger Delta, where most of the crude oil in Nigeria is found. The isolated strain was able to utilize Bonny light crude oil, diesel, and kerosene, generating organic acids. The finding is promising for this region, where the oil spills are a source of significant air, soil, and water pollution, destroying biodiversity in the ecosystem [<xref ref-type="bibr" rid="CR105">105</xref>]. Lutz et al<italic>.</italic> [<xref ref-type="bibr" rid="CR78">78</xref>] described a wild-type bacterial cocktail marketed as Superbugs<sup>®</sup> and composed of bacteria belonging to genera <italic>Proteus</italic>, <italic>Bacillus</italic>, <italic>Pseudomonas</italic>, <italic>Citrobacter</italic>, and <italic>Enterobacter</italic>, as effective in the biodegradation of ethyl biodiesel made from palm triacylglycerols in Costa Rica.</p><p>There are several reports on <italic>Proteus</italic> spp. strains able to biodegrade polyaromatic hydrocarbons (PAHs). The genus <italic>Proteus</italic> dominated after <italic>E. coli</italic> in the group of 60 different bacterial strains able to degrade hydrocarbons, classified as hazardous waste in soil (benzene, toluene, octane, heptanes, biphenyl, naphthalene, camphor, and phenanthrene), isolated from soil samples near different petrol pumps of Karachi City, Pakistan [<xref ref-type="bibr" rid="CR139">139</xref>]. The genes responsible for the hydrocarbon degradation ability were located either chromosomally or extra-chromosomally. The plasmid location is promising for bioremediation processes since the genes can be conjugated to other microorganisms in polluted environments. Ceyhan [<xref ref-type="bibr" rid="CR22">22</xref>] reported on a <italic>P. vulgaris</italic> strain, isolated from biofilm in wastewater of the petrochemical industry in Turkey, which was effective in the degradation of pyrene (four-ring PAH) as a sole source of carbon and energy. Moreover, the degradation of this highly toxic and carcinogenic hydrocarbon resulted in non-toxic and non-accumulating metabolites, proving a big biodegradation potential of the strain.</p><p>Gasoline-contaminated soil from a gas station in Chihuahua, Mexico, was the habitat of a <italic>P. mirabilis</italic> strain degrading with medium efficiency methyl tert-butyl ether (MTBE), which is a toxic synthetic compound added to gasoline in a high concentration of 15 %, as a blending component [<xref ref-type="bibr" rid="CR90">90</xref>]. Next, a <italic>P. mirabilis</italic> strain was found, which was able to efficiently degrade phenol as a sole carbon and energy source in an oil-contaminated soil sample collected in India [<xref ref-type="bibr" rid="CR88">88</xref>]. Sanuth et al<italic>.</italic> [<xref ref-type="bibr" rid="CR128">128</xref>] identified a <italic>P. mirabilis</italic> strain which was the most effective in ɛ-caprolactam degradation among the bacteria isolated from soils collected from the major solid waste dumpsites in Lagos State, Nigeria. ɛ-Caprolactam is a monomer for nylon-6 production, found in wastewater effluents from nylon-producing factories, toxic to plants, animals, and humans. The strain seems to be a potential candidate for its bioremediation.</p><p>Bacteria from the genus <italic>Proteus</italic> solely or in consortia also display an ability to neutralize different toxic herbicides and pesticides that may cause heavy pollution in terrestrial and aquatic ecosystems, especially when inappropriately used. <italic>P. vulgaris</italic> from a mouse intestine was one of the first reported bacteria solely able to reduce dichloro-diphenyl-trichloroethane (DDT) pesticide to dichloro-diphenyl-dichloroethane (DDD) [<xref ref-type="bibr" rid="CR41">41</xref>]. Although DDD is also a toxic pesticide, its production is the first step during the degradation and mineralization of DDT, and it is utilized in further transformations.</p><p>Correa and Steen [<xref ref-type="bibr" rid="CR27">27</xref>] found a <italic>P. mirabilis</italic> strain to be the fastest degrader of the propanil (a commonly used herbicide) among the natural microflora inhabiting a pristine lake in northeast Georgia, USA, followed by the bacteria belonging to the genera <italic>Aeromonas</italic>, <italic>Aerobacter</italic>, and <italic>Acinetobacter</italic>.</p><p><italic>Proteus</italic> spp. bacteria isolated from the rhizosphere of rice in West Bengal, India, used hexachlorocyclohexane (HCH) pesticide [<xref ref-type="bibr" rid="CR30">30</xref>] or phorate insecticide [<xref ref-type="bibr" rid="CR31">31</xref>, <xref ref-type="bibr" rid="CR32">32</xref>] as a source of carbon and energy, and the addition of these chemicals to soil intensified the growth of bacteria. It is worth mentioning that <italic>Proteus</italic> spp. were the only members of the family <italic>Enterobacteriaceae</italic> isolated from these soil samples besides typical soil bacteria, actinomycetes, and fungi. Another example of autochthonous <italic>Proteus</italic> sp. strain, isolated from phorate-contaminated soil in India and able to degrade this insecticide, was described by Bano and Musarrat [<xref ref-type="bibr" rid="CR11">11</xref>]. The strain exhibited also siderophore production, phosphate solubilizing capacities, and strong antifungal effect on phytopathogen <italic>Fusarium oxysporum</italic>, thus indicating the potential possibilities of its exploitation as PGPR as well.</p><p>The presence of <italic>P. vulgaris</italic> and <italic>Proteus</italic> sp. strains in microbial consortia capable of pesticide degradation was detected in highly contaminated soils in Colombia [<xref ref-type="bibr" rid="CR116">116</xref>]. From soil samples exposed to different kinds of waste (including hazardous ones), a microbial consortium was isolated composed of ten strains, including <italic>P. vulgaris</italic> and <italic>Proteus</italic> sp. The consortium was able to degrade two widely used organophosphatic pesticides, chlorpyrifos and methyl parathion, both in culture medium and in soil. A similar bacterial consortium was found in highly contaminated soil samples from Moravia, Medellin, an area that was used as a garbage dump from 1974 to 1982 [<xref ref-type="bibr" rid="CR115">115</xref>]. The consortium was able to degrade methyl parathion and p-nitrophenol as the only source of carbon and to decrease their toxicity in the medium and in soil at different depths.</p><p>Azo dyes frequently used for textile dyeing and paper printing and their metabolites present in effluents may be toxic, mutagenic, or carcinogenic. Their physicochemical neutralization is costly, while biological degradation is cost-effective and friendly to the environment, but difficult. For that reason, identification of the effective <italic>Proteus</italic> spp. degraders is a promising perspective for the environmental protection. Patil et al<italic>.</italic> [<xref ref-type="bibr" rid="CR112">112</xref>] have isolated a <italic>Proteus</italic> sp. strain (related to <italic>P. vulgaris</italic>) from a waste site of the textile industry in India, which was capable of degrading seven textile azo dyes, but the most effective decolorization and detoxification of Navy Blue Rx were observed due to the induction of laccase and other enzymes. Chen et al<italic>.</italic> [<xref ref-type="bibr" rid="CR25">25</xref>] isolated from sludge, obtained from a dyeing wastewater treatment plant in Taiwan, a <italic>P. mirabilis</italic> strain exhibiting a great capacity of efficient enzymatic reduction and decolorization associated with the biosorption of deep red RED RBN as well as deep black BK-5 azo dyes. Furthermore, Olukanni et al<italic>.</italic> [<xref ref-type="bibr" rid="CR106">106</xref>] isolated from municipal dump site soil near Lagos, Nigeria, a <italic>P. mirabilis</italic> strain able to degrade a Reactive Blue 13 azo dye to phyto-non-toxic products. However, its laccase (the azo-dye-degrading oxidoreductase) activity was 70-fold lower than that of another very effective strain, <italic>P. hauseri</italic>, isolated from the Chiao-His hot spring in Taiwan [<xref ref-type="bibr" rid="CR95">95</xref>, <xref ref-type="bibr" rid="CR157">157</xref>]. It effectively decolorized several mono- and di-azo dyes [<xref ref-type="bibr" rid="CR23">23</xref>, <xref ref-type="bibr" rid="CR24">24</xref>] and was copper-tolerant as its laccase was a copper-induced enzyme with thermophilic and acidophilic properties [<xref ref-type="bibr" rid="CR159">159</xref>]. However, the presence of copper in the environment reduced the swarming activity of the bacterium [<xref ref-type="bibr" rid="CR96">96</xref>]. The isolate is the first reported non-pathogenic strain in the species <italic>P. hauseri</italic>, coming from natural water habitat.</p><p>There are more reports on the high tolerance of <italic>Proteus</italic> spp. bacteria to copper and other heavy metals. Ge et al<italic>.</italic> [<xref ref-type="bibr" rid="CR45">45</xref>], from the East Sea (China) contaminated by chromate, isolated a <italic>Proteus</italic> sp. strain (related to <italic>P. penneri</italic> and <italic>P. hauseri</italic>) which was highly tolerant to Cr (VI) and could significantly reduce the amounts of this toxic metal in seawater. Hassen et al<italic>.</italic> [<xref ref-type="bibr" rid="CR55">55</xref>] in Tunisia isolated from wastewater many Gram-negative bacteria with dominating <italic>Pseudomonas</italic> spp. and <italic>P. mirabilis</italic> strains, highly tolerant especially to copper and also to chromium, cobalt, cadmium, zinc, and mercury. Also, a highly resistant to several heavy metals (including mercury, copper, zinc, cadmium, cobalt, silver, and others) <italic>P. mirabilis</italic> strain was identified in wastewater samples from Casablanca City, Moroccco, also exhibiting resistance to naphthalene, anthracene, and antibiotics [<xref ref-type="bibr" rid="CR40">40</xref>]. Another strongly copper resistant strain identified as <italic>P. vulgaris</italic> and isolated from soil samples collected near the Panki power plant in Kampur, India, was reported by Rani et al<italic>.</italic> [<xref ref-type="bibr" rid="CR120">120</xref>]. The strain used to inoculate pigeon pea (<italic>Cajanus cajan</italic>) seeds protected the pea against the inhibitory effect of copper, reducing its amounts both in soil and in the plant. Moreover, the bacterium was able to produce siderophores providing pigeon pea with iron and preventing chlorosis.</p><p>There are more examples of soil <italic>Proteus</italic> spp. strains beneficial to plants (Table <xref rid="Tab3" ref-type="table">3</xref>). Islam et al<italic>.</italic> [<xref ref-type="bibr" rid="CR60">60</xref>] reported on a <italic>P. mirabilis</italic> strain highly resistant to zinc, found in agricultural field soil, irrigated with industrial effluents in Faisalabad City, Pakistan. The strain was able to block zinc absorption by maize (<italic>Zea mays</italic>) roots, reduce oxidative stress in the plant, and increase its tolerance to zinc, promoting maize growth in the presence of the heavy metal. Simultaneously, the bacterium enhanced phytoremediation processes conducted by this copper-resistant plant. Rau et al. [<xref ref-type="bibr" rid="CR121">121</xref>] characterized a <italic>P. mirabilis</italic> strain isolated from rhizosphere of wild grass <italic>Saccharum ravennae</italic> colonizing fly ash dumps in Delhi, India. The strain displayed strong resistance to arsenic and was medium resistant to copper, chromium, cobalt, cadmium, zinc, mercury, nickel, and lead. Additionally, the strain produced siderophores with great capacity and was an active phosphate solubilizer, thus enhancing the growth of grass. Similarly, a <italic>Proteus</italic> sp. strain from a rice field in Pakistan inoculated on wheat seeds effectively solubilized rock phosphate composted with poultry litter, stimulating the plant growth [<xref ref-type="bibr" rid="CR14">14</xref>]. Yet, rhizobacterial <italic>P. vulgaris</italic> strains, identified in acidic soil from a tea (<italic>Camellia sinensis</italic>) plantation in India, expressed siderophore production and antifungal properties both in acidic and in neutral pH conditions [<xref ref-type="bibr" rid="CR12">12</xref>]. The strains successfully protected three tested species of leguminous plants from the pathogenic fungus <italic>Fusarium moniliformae</italic>; when the seeds were bacterized during the sowing, they were able to colonize roots and promote the growth of host plants. Lu et al<italic>.</italic> [<xref ref-type="bibr" rid="CR76">76</xref>] found in cow dung in China <italic>P. penneri</italic> strains which produced volatile organic compounds killing within 1 h 98–100 % of tested nematodes: soil <italic>Caenorhabditis elegans</italic> and plant-pathogenic <italic>Meloidogyne incognita</italic>, thus expressing the possibility of being used as a protecting plant biocontrol agent. Yu and Lee [<xref ref-type="bibr" rid="CR156">156</xref>] stated that indole production by the <italic>P. vulgaris</italic> strain (Table <xref rid="Tab1" ref-type="table">1</xref>) isolated from the rhizosphere of halophyte glasswort (<italic>Salicornia herbacea</italic> L.) effectively promoted the growth of Chinese cabbage seedling (<italic>Brassica campestris</italic> ssp. <italic>pekinensis</italic>), while Bhattacharyya et al<italic>.</italic> [<xref ref-type="bibr" rid="CR13">13</xref>] reported that the same strain stimulated the growth of <italic>Arabidopsis thaliana</italic> (a small flowering plant from the family <italic>Brassicacae</italic>) by indole production influencing the auxin, cytokinin, and brassinosteroid signaling pathways.</p><p>These promising results open wider possibilities of using specialized <italic>Proteus</italic> spp. strains as bioremediators and PGPR.</p></sec><sec id="Sec7" sec-type="conclusion"><title>Conclusion</title><p>Bacteria from the genus <italic>Proteus</italic> are well known as human opportunistic pathogens and intestinal microorganisms indicating fecal pollution of water or soil. Their presence in drinking water poses a threat of infection. On the other hand, the bacilli are believed to play an important role in removing organic pollutants of animal origin, especially fecal ones, by decomposing the dead organic matter in water or soil environments. Their proteolytic and ureolytic properties may place the bacteria among the most efficient saprobes taking part in the enrichment of manured soils in ammonia salts and therefore participating in the nitrogen cycle. However, the significance of these microorganisms in the mineralization processes of nitrogen-containing organic compounds is not obvious. This aspect of their metabolism requires more research. It would be reasonable to establish their exact contribution as destruents to the circulation of matter in nature.</p><p><italic>Proteus</italic> spp. strains are sometimes found to co-operate with higher organisms, playing a role of animal and plant symbionts. Their antagonistic or commensal relationships with numerous animals have also been documented. However, environments other than the human body are less recognized as habitats of <italic>Proteus</italic> spp. rods. In the future, more attention should be paid to the interdependences between <italic>Proteus</italic> spp. and animals or plants coexisting with the bacteria in the environment. Relatively little information is available also about the mutual relations between <italic>Proteus</italic> spp. bacilli and other bacteria in natural habitats. Establishing what kind of relationships these are and which organisms benefit from this system is the basis for determining the reasons why the bacilli occur in a given ecosystem and the consequences of their activity.</p><p>Nowadays, molecular techniques provide proper tools to investigate the microorganisms in their natural habitats. The differences in the biochemical features do not exclude the strain from a genus as long as the similarities on the genome level are big enough. It is important to employ molecular techniques in the identification of <italic>Proteus</italic> spp. strains, especially those belonging to the new genomospecies, the biochemical differentiation of which is impossible. Metagenomic analysis of soil and water environments as well as of different niches in human, animal, and plant organisms using proper primer sequences may reveal the presence of <italic>Proteus</italic> spp. strains in these habitats even if they exhibit atypical activities and play unusual roles.</p><p><italic>Proteus</italic> spp. bacteria often display exceptional metabolic features, allowing them to adapt to various conditions and reach distant niches in natural environments where they may be recognized as autochthons. Although the genus is usually not mentioned among PGPR or bioremediators, <italic>Proteus</italic> spp. environmental strains possess the abilities of immobilization of heavy metals, utilization of toxic pollutants, and plant growth stimulation, as well as nematicidal and fungicidal properties. Numerous examples suggest that the application of these microorganisms may be an effective way of protecting plants and groundwater. The biological treatment of polluted natural environments is more efficient and cost-effective than physicochemical methods and can be used in large areas due to simple application and an ability to remove pollution completely. Bioremediation could involve not only the stimulation of the natural autochthonic <italic>Proteus</italic> spp. strains but also introducing these microorganisms to the polluted environment.</p><p>However, it is important to remember that the bacteria belonging to the genus <italic>Proteus</italic> are opportunistic human and animal pathogens. It would be useful and interesting to compare the features (especially virulence factors, serotypes, metabolic apparatus, and the antibiotic resistance) expressed by <italic>Proteus</italic> spp. clinical isolates and by the strains existing in animal, soil, and water ecosystems. Do environmental <italic>Proteus</italic> spp. strains differ significantly from clinical ones? Do they possess genes coding the factors of pathogenicity identified in the strains isolated from patients? If so, do they express these factors and how do they use them in non-pathogenic conditions? What is the risk of transformation of a strain which could be used in bioremediation and environmental protection into a virulent one posing a threat to the animals or humans inhabiting the area? Do the environmental strains carry antibiotic resistance genes, which might lead to the transfer of these genes into other microorganisms in the environment? Answers to these questions could explain which factors contribute to and in what way they are important in different lifestyles presented by <italic>Proteus</italic> spp. bacteria in various environments.</p></sec></body><back><ack><p>I thank Prof. Antoni Różalski for critical reading of the manuscript.</p></ack><ref-list id="Bib1"><title>References</title><ref id="CR1"><label>1.</label><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Aboh</surname><given-names>EA</given-names></name><name><surname>Giwa</surname><given-names>FJ</given-names></name><name><surname>Giwa</surname><given-names>A</given-names></name></person-group><article-title>Microbiological assessment of well waters in Samaru, Zaria, Kaduna, State, Nigeria</article-title><source>Ann Afr Med</source><year>2015</year><volume>14</volume><fpage>32</fpage><lpage>38</lpage><pub-id pub-id-type="doi">10.4103/1596-3519.148732</pub-id><pub-id 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