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<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">Accurate differentiation of <italic>Escherichia coli</italic> and <italic>Shigella</italic> serogroups: challenges and strategies</title><author><name sortKey="Devanga Ragupathi, N K" sort="Devanga Ragupathi, N K" uniqKey="Devanga Ragupathi N" first="N. K." last="Devanga Ragupathi">N. K. Devanga Ragupathi</name></author><author><name sortKey="Muthuirulandi Sethuvel, D P" sort="Muthuirulandi Sethuvel, D P" uniqKey="Muthuirulandi Sethuvel D" first="D. P." last="Muthuirulandi Sethuvel">D. P. Muthuirulandi Sethuvel</name></author><author><name sortKey="Inbanathan, F Y" sort="Inbanathan, F Y" uniqKey="Inbanathan F" first="F. Y." last="Inbanathan">F. Y. Inbanathan</name></author><author><name sortKey="Veeraraghavan, B" sort="Veeraraghavan, B" uniqKey="Veeraraghavan B" first="B." last="Veeraraghavan">B. Veeraraghavan</name></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">29204286</idno><idno type="pmc">5711669</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5711669</idno><idno type="RBID">PMC:5711669</idno><idno type="doi">10.1016/j.nmni.2017.09.003</idno><date when="2017">2017</date><idno type="wicri:Area/Pmc/Corpus">001391</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Corpus" wicri:corpus="PMC">001391</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Accurate differentiation of <italic>Escherichia coli</italic> and <italic>Shigella</italic> serogroups: challenges and strategies</title><author><name sortKey="Devanga Ragupathi, N K" sort="Devanga Ragupathi, N K" uniqKey="Devanga Ragupathi N" first="N. K." last="Devanga Ragupathi">N. K. Devanga Ragupathi</name></author><author><name sortKey="Muthuirulandi Sethuvel, D P" sort="Muthuirulandi Sethuvel, D P" uniqKey="Muthuirulandi Sethuvel D" first="D. P." last="Muthuirulandi Sethuvel">D. P. Muthuirulandi Sethuvel</name></author><author><name sortKey="Inbanathan, F Y" sort="Inbanathan, F Y" uniqKey="Inbanathan F" first="F. Y." last="Inbanathan">F. Y. Inbanathan</name></author><author><name sortKey="Veeraraghavan, B" sort="Veeraraghavan, B" uniqKey="Veeraraghavan B" first="B." last="Veeraraghavan">B. Veeraraghavan</name></author></analytic><series><title level="j">New Microbes and New Infections</title><idno type="eISSN">2052-2975</idno><imprint><date when="2017">2017</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p><italic>Shigella</italic> spp. and <italic>Escherichia coli</italic> are closely related; both belong to the family <italic>Enterobacteriaceae.</italic> Phenotypically, <italic>Shigella</italic> spp. and <italic>E. coli</italic> share many common characteristics, yet they have separate entities in epidemiology and clinical disease, which poses a diagnostic challenge. We collated information for the best possible approach to differentiate clinically relevant <italic>E. coli</italic> from <italic>Shigella</italic> spp. We found that a molecular approach is required for confirmation. High discriminatory potential is seen with whole genome sequencing analysed for k-mers and single nucleotide polymorphism. Among these, identification using single nucleotide polymorphism is easy to perform and analyse, and it thus appears more promising. Among the nonmolecular methods, matrix-assisted desorption ionization–time of flight mass spectrometry may be applicable when data analysis is assisted with advanced analytic tools.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Brenner, D J" uniqKey="Brenner D">D.J. Brenner</name></author><author><name sortKey="Fanning, G R" uniqKey="Fanning G">G.R. Fanning</name></author><author><name sortKey="Steigerwalt, A G" uniqKey="Steigerwalt A">A.G. Steigerwalt</name></author><author><name sortKey="Orskov, I" uniqKey="Orskov I">I. Orskov</name></author><author><name sortKey="Orskov, F" uniqKey="Orskov F">F. 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<front><journal-meta><journal-id journal-id-type="nlm-ta">New Microbes New Infect</journal-id><journal-id journal-id-type="iso-abbrev">New Microbes New Infect</journal-id><journal-title-group><journal-title>New Microbes and New Infections</journal-title></journal-title-group><issn pub-type="epub">2052-2975</issn><publisher><publisher-name>Elsevier</publisher-name></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">29204286</article-id><article-id pub-id-type="pmc">5711669</article-id><article-id pub-id-type="publisher-id">S2052-2975(17)30074-4</article-id><article-id pub-id-type="doi">10.1016/j.nmni.2017.09.003</article-id><article-categories><subj-group subj-group-type="heading"><subject>Mini-Review</subject></subj-group></article-categories><title-group><article-title>Accurate differentiation of <italic>Escherichia coli</italic> and <italic>Shigella</italic> serogroups: challenges and strategies</article-title></title-group><contrib-group><contrib contrib-type="author"><name><surname>Devanga Ragupathi</surname><given-names>N.K.</given-names></name></contrib><contrib contrib-type="author"><name><surname>Muthuirulandi Sethuvel</surname><given-names>D.P.</given-names></name></contrib><contrib contrib-type="author"><name><surname>Inbanathan</surname><given-names>F.Y.</given-names></name></contrib><contrib contrib-type="author"><name><surname>Veeraraghavan</surname><given-names>B.</given-names></name><email>vbalaji@cmcvellore.ac.in</email><xref rid="cor1" ref-type="corresp">∗</xref></contrib></contrib-group><aff id="aff1">Department of Clinical Microbiology, Christian Medical College, Vellore, India</aff><author-notes><corresp id="cor1"><label>∗</label>Corresponding author. B. Veeraraghavan, Department of Clinical Microbiology, Christian Medical College, Vellore 4, IndiaDepartment of Clinical MicrobiologyChristian Medical CollegeVellore4India <email>vbalaji@cmcvellore.ac.in</email></corresp></author-notes><pub-date pub-type="pmc-release"><day>23</day><month>9</month><year>2017</year></pub-date><pmc-comment> PMC Release delay is 0 months and 0 days and was based on .</pmc-comment>
<pub-date pub-type="collection"><month>1</month><year>2018</year></pub-date><pub-date pub-type="epub"><day>23</day><month>9</month><year>2017</year></pub-date><volume>21</volume><fpage>58</fpage><lpage>62</lpage><history><date date-type="received"><day>28</day><month>6</month><year>2017</year></date><date date-type="rev-recd"><day>7</day><month>9</month><year>2017</year></date><date date-type="accepted"><day>19</day><month>9</month><year>2017</year></date></history><permissions><copyright-statement>© 2017 The Authors</copyright-statement><copyright-year>2017</copyright-year><license license-type="CC BY-NC-ND" xlink:href="http://creativecommons.org/licenses/by-nc-nd/4.0/"><license-p>This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).</license-p></license></permissions><abstract id="abs0010"><p><italic>Shigella</italic> spp. and <italic>Escherichia coli</italic> are closely related; both belong to the family <italic>Enterobacteriaceae.</italic> Phenotypically, <italic>Shigella</italic> spp. and <italic>E. coli</italic> share many common characteristics, yet they have separate entities in epidemiology and clinical disease, which poses a diagnostic challenge. We collated information for the best possible approach to differentiate clinically relevant <italic>E. coli</italic> from <italic>Shigella</italic> spp. We found that a molecular approach is required for confirmation. High discriminatory potential is seen with whole genome sequencing analysed for k-mers and single nucleotide polymorphism. Among these, identification using single nucleotide polymorphism is easy to perform and analyse, and it thus appears more promising. Among the nonmolecular methods, matrix-assisted desorption ionization–time of flight mass spectrometry may be applicable when data analysis is assisted with advanced analytic tools.</p></abstract><kwd-group id="kwrds0010"><title>Keywords</title><kwd>16S rRNA</kwd><kwd>k-mer</kwd><kwd>MALDI-TOF MS</kwd><kwd>single nucleotide polymorphism</kwd><kwd>whole genome sequencing</kwd></kwd-group></article-meta></front><body><sec id="sec1"><title>Introduction</title><p id="p0010">Diarrhoeal disease is not uncommon in both developing and developed countries. <italic>Shigella</italic> spp. are among the most important enteric pathogens causing bacillary dysentery worldwide, mainly in humans. Differentiation of <italic>Shigella</italic> spp. from <italic>Escherichia coli</italic> is challenging because of their close genetic relatedness. Brenner <italic>et al.</italic><xref rid="bib1" ref-type="bibr">[1]</xref> determined that the nucleotide similarity between <italic>Shigella</italic> and <italic>E. coli</italic> was 80% to 90%, whereas other <italic>Escherichia</italic> species are genetically distant <xref rid="bib2" ref-type="bibr">[2]</xref>. <italic>Shigellae</italic> are phylogenetically <italic>E. coli</italic> that were later classified as separate species on the bases of biochemical characteristics and clinical relevance <xref rid="bib3" ref-type="bibr">[3]</xref>, <xref rid="bib4" ref-type="bibr">[4]</xref>.</p><p id="p0015">Biochemical characteristics and serotyping are usually used to identify the species. However, many isolates cannot be distinguished as either <italic>E. coli</italic> or <italic>Shigella</italic> spp. Molecular methods such as 16S rRNA gene sequencing and protein signature–based matrix-assisted laser desorption/ionization–time of flight mass spectrometry (MALDI-TOF MS) are unable to differentiate <italic>Shigella</italic> spp. from <italic>E. coli</italic><xref rid="bib4" ref-type="bibr">[4]</xref>. Further, <italic>Shigella</italic>-like strains of <italic>E. coli</italic> (enteroinvasive <italic>E. coli</italic>, EIEC) causing invasive dysenteric diarrhoeal illness make clinical and laboratory diagnoses difficult. In addition, the change in antimicrobial resistance patterns with the change in the serogroup/serotype further highlights the need for accurate identification of <italic>Shigella</italic> spp. so that appropriate antimicrobial therapy may be administered <xref rid="bib5" ref-type="bibr">[5]</xref>.</p><p id="p0020">We attempted to accurately identify <italic>E. coli</italic> and <italic>Shigella</italic> spp., and trace the evolution of facts contributing to the masking of discrimination between <italic>E. coli</italic> and <italic>Shigella</italic> spp. We discuss the challenges and the possible methods to differentiate <italic>E. coli</italic> and <italic>Shigella</italic> spp. using protein signature and molecular tools.</p></sec><sec id="sec2"><title>Evolution of <italic>Shigella</italic> Species</title><p id="p0025">At present, <italic>Shigella</italic> and <italic>Escherichia</italic> genera are considered to be unique genomospecies. Unlike <italic>E. coli, Shigella</italic> strains are nonmotile as a result of deletion in the <italic>fliF</italic> operon (flagellar coding region) or an IS<italic>I</italic> insertion mutation in the <italic>flhD</italic> operon. Also, <italic>Shigella</italic> does not ferment lactose, as <italic>S. flexneri</italic><xref rid="bib1" ref-type="bibr">[1]</xref>, <xref rid="bib3" ref-type="bibr">[3]</xref> and <italic>S. bodyii</italic><xref rid="bib2" ref-type="bibr">[2]</xref>, <xref rid="bib4" ref-type="bibr">[4]</xref> do not contain any of the <italic>lac</italic> genes (<italic>lac</italic>Y, <italic>lac</italic>A and <italic>lac</italic>Z) required for fermentation. <italic>S. dysenteriae</italic> 1 was known to have only <italic>lac</italic>Y and <italic>lac</italic>A. <italic>S. sonnei</italic> has all three genes but is unable to ferment as a result of lack of permease activity. These observations are one such example for the multiple origins of the <italic>Shigella</italic> phenotype by convergent evolution <xref rid="bib6" ref-type="bibr">[6]</xref>.</p><p id="p0030">Earlier reports suggested that the arrival of a virulence plasmid into an <italic>E. coli</italic> strain gave rise to a monophyletic group from which all <italic>Shigella</italic> and <italic>E. coli</italic> groups descended. This led to the occurrence of highly diversified and pathogenic virotypes, which includes EIEC, Shiga toxin–producing <italic>E. coli</italic> (STEC; includes enterohemorrhagic <italic>E. coli</italic>, EHEC), enteropathogenic <italic>E. coli</italic> (EPEC), enteroaggregative <italic>E. coli</italic> (EAEC) and enterotoxigenic <italic>E. coli</italic> (ETEC) <xref rid="bib7" ref-type="bibr">[7]</xref>. Interestingly, commensal <italic>E. coli</italic> strains may not become pathogenic <italic>Shigella</italic> on acquiring a virulence plasmid, as it does not seem to transmit horizontally among <italic>E. coli</italic> and <italic>Shigella</italic> strains <xref rid="bib7" ref-type="bibr">[7]</xref>.</p><p id="p0035">STEC that is able to cause haemorrhagic colitis and haemolytic uremic syndrome is referred to as EHEC. This causes pancolitis due to toxigenic noninvasive (EHEC) infection, whereas EIEC causes proctocolitis via a nontoxigenic invasive mechanism similar to <italic>Shigella</italic><xref rid="bib8" ref-type="bibr">[8]</xref>. EIEC serotypes have been suggested as being ancestral to the different <italic>Shigella</italic> serogroups contributing to these differences <xref rid="bib9" ref-type="bibr">[9]</xref>. However, supporting evidence for evolution of STEC is not clear. Similarly, limited information is available on the origins of other virotypes of <italic>E. coli.</italic></p><p id="p0040">In the midst of changing evolution, there is a need for accurate identification of <italic>E. coli</italic> and <italic>Shigella</italic> spp. for appropriate clinical management and accurate epidemiologic data. The accuracy of identification using molecular methods (duplex real-time PCR, 16S rRNA, multilocus sequence typing (MLST) and whole genome sequencing (WGS)) and nonmolecular methods (matrix-assisted desorption ionization–time of flight mass spectrometry, MALDI-TOF MS) will be discussed.</p></sec><sec id="sec3"><title>Currently Used Molecular Methods for Differentiation of <italic>E. coli</italic> and <italic>Shigella</italic> spp.</title><sec id="sec3.1"><title>Duplex real-time PCR</title><p id="p0045">A duplex real-time PCR for differentiation of EIEC and <italic>Shigella</italic> spp. was reported by Pavlovic <italic>et al.</italic><xref rid="bib10" ref-type="bibr">[10]</xref>; this PCR amplified the genes encoding β-glucuronidase (<italic>uid</italic>A) and lactose permease (<italic>lac</italic>Y). The gene <italic>uid</italic>A is common for <italic>E. coli</italic> and <italic>Shigella,</italic> while the latter (<italic>lac</italic>Y) is present only in <italic>E. coli.</italic> Ninety-six isolates including 11 EIEC isolates of different serotypes and at least three representatives of each <italic>Shigella</italic> species were identified correctly. Likewise, Lobersli <italic>et al.</italic><xref rid="bib11" ref-type="bibr">[11]</xref> established a duplex real-time PCR (<italic>ipa</italic>H and <italic>lac</italic>Y) to differentiate EIEC and <italic>Shigella</italic> spp., where <italic>lac</italic>Y is specific to <italic>E. coli.</italic> This PCR target differentiated <italic>Shigella</italic> spp. and EIEC O121 and O124 groups, but not EIEC O164 group.</p></sec><sec id="sec3.2"><title>16S rRNA gene sequencing to differentiate <italic>E. coli</italic> from <italic>Shigella</italic> spp.</title><p id="p0050">Molecular identification using 16S rRNA sequencing could not distinguish atypical <italic>E. coli</italic> and <italic>Shigella</italic> spp. <xref rid="bib12" ref-type="bibr">[12]</xref>, <xref rid="bib13" ref-type="bibr">[13]</xref>. The 16S rRNA sequence similarities between various pathogenic strains of <italic>E. coli,</italic> EPEC (KR476716), EHEC (CP018252), STEC (CP015229), EIEC (AB604198), <italic>E. coli</italic> ATCC 25922 (KC429776), <italic>S. boydii</italic> (JQ073777), <italic>S. sonnei</italic> (HQ591457), <italic>S. flexneri</italic> (NR026331)<italic>, S. flexneri</italic> 2a (CP012137)<italic>, S. flexneri</italic> 5a (NZCM001474) and <italic>S. dysenteriae</italic> (NR026332) were calculated using the available reference 16S rRNA sequences from the National Center for Biotechnology Information (NCBI) database (<xref rid="tbl1" ref-type="table">Table 1</xref>).<table-wrap id="tbl1" position="float"><label>Table 1</label><caption><p>16S rRNA sequence similarity between closely related <italic>Shigella</italic> serogroups, serotypes and virotypes of <italic>Escherichia coli</italic></p></caption><alt-text id="alttext0015">Table 1</alt-text><table frame="hsides" rules="groups"><thead><tr><th></th><th><italic>E. coli</italic> ATCC 25922</th><th>EPEC</th><th>EHEC</th><th>STEC</th><th>EIEC</th><th><italic>S. dysenteriae</italic></th><th><italic>S. flexneri</italic> 2a</th><th><italic>S. flexneri</italic> 5a</th><th><italic>S. flexneri</italic></th><th><italic>S. boydii</italic></th><th><italic>S. sonnei</italic></th></tr></thead><tbody><tr><td><italic>E. coli</italic> ATCC 25922</td><td>100</td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td></tr><tr><td>EPEC</td><td>98.89</td><td>100</td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td></tr><tr><td>EHEC</td><td>99.04</td><td>98.89</td><td>100</td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td></tr><tr><td>STEC</td><td>98.97</td><td>98.55</td><td>99.42</td><td>100</td><td></td><td></td><td></td><td></td><td></td><td></td><td></td></tr><tr><td>EIEC</td><td>99.63</td><td>98</td><td>98.41</td><td>98.47</td><td>100</td><td></td><td></td><td></td><td></td><td></td><td></td></tr><tr><td><italic>S. dysenteriae</italic></td><td>98.97</td><td>98.2</td><td>98.92</td><td>98.99</td><td>98.72</td><td>100</td><td></td><td></td><td></td><td></td><td></td></tr><tr><td><italic>S. flexneri</italic> 2a</td><td>99.63</td><td>98.06</td><td>98.91</td><td>98.97</td><td>99.53</td><td>98.86</td><td>100</td><td></td><td></td><td></td><td></td></tr><tr><td><italic>S. flexneri</italic> 5a</td><td>99.63</td><td>98</td><td>98.84</td><td>99.03</td><td>99.07</td><td>98.92</td><td>99.55</td><td>100</td><td></td><td></td><td></td></tr><tr><td><italic>S. flexneri</italic></td><td>99.78</td><td>98.2</td><td>98.99</td><td>99.13</td><td>99.6</td><td>99.13</td><td>99.73</td><td>99.8</td><td>100</td><td></td><td></td></tr><tr><td><italic>S. boydii</italic></td><td>99.56</td><td>98</td><td>98.8</td><td>98.87</td><td>99.66</td><td>98.79</td><td>99.93</td><td>99.47</td><td>99.66</td><td>100</td><td></td></tr><tr><td><italic>S. sonnei</italic></td><td>99.56</td><td>97.93</td><td>98.78</td><td>98.97</td><td>99</td><td>98.86</td><td>99.49</td><td>99.68</td><td>99.73</td><td>99.4</td><td>100</td></tr></tbody></table><table-wrap-foot><fn><p>EHEC, enterohaemorrhagic <italic>E. coli</italic>; EIEC, enteroinvasive <italic>E. coli</italic>; EPEC, enteropathogenic <italic>E. coli</italic>; STEC, Shiga toxin–producing <italic>E. coli.</italic></p></fn></table-wrap-foot></table-wrap></p><p id="p0055">The differentiation of <italic>E. coli</italic> and <italic>Shigella</italic> spp. could not be achieved using 16S rRNA gene sequences as a result of the narrow (<1%) divergence between EHEC, EIEC and <italic>Shigella</italic> spp. Jenkins <italic>et al.</italic><xref rid="bib14" ref-type="bibr">[14]</xref> concur with this finding; their 16S rRNA gene comparison could not distinguish between <italic>E. coli</italic> and <italic>Shigella</italic> spp. as a result of >99% sequence identity. We therefore deem this approach to be unacceptable to differentiate certain inter- and intraspecies identity.</p></sec><sec id="sec3.3"><title>Exploration of MLST for differentiation of <italic>E. coli</italic> and <italic>Shigella</italic> spp.</title><p id="p0060">The Pasteur and Warwick MLST databases use highly conserved housekeeping genes that are the same for both <italic>E. coli</italic> and <italic>Shigella</italic> spp. Hence, sequence types are assigned irrespective of <italic>E. coli</italic> and <italic>Shigella</italic> spp. A study by Li <italic>et al.</italic><xref rid="bib15" ref-type="bibr">[15]</xref> involving MLST for clinical <italic>S. flexneri</italic> isolates found that different serotypes (1–5, X and Y) were clustered together in a group, while a single serotype formed a distinct group. Li <italic>et al.</italic> reported the inability of MLST method to differentiate the evolutionary relationship between virotypes of <italic>E. coli</italic> and <italic>Shigella</italic> spp. However, there have been reports focusing directly on sequence data from the housekeeping genes rather than the allelic profile for clonal diversification. The discrimination based on difference in one MLST housekeeping gene sequence from the founder genotype is termed single-locus variants, and diversification of two housekeeping genes is defined as double-locus variants (DLVs) <xref rid="bib16" ref-type="bibr">[16]</xref>, <xref rid="bib17" ref-type="bibr">[17]</xref>, <xref rid="bib18" ref-type="bibr">[18]</xref>, <xref rid="bib19" ref-type="bibr">[19]</xref>. Until now, these variants were used to categorize clonal complexes to relate the phylogeny. Taking a cue from this knowledge, we made an attempt to use the direct sequence data of housekeeping genes to differentiate <italic>E. coli</italic> from <italic>Shigella</italic> spp.</p><p id="p0065">Interestingly, we could identify the variations among <italic>Shigella</italic> spp. and <italic>E. coli</italic> virotypes beyond their sequence types utilizing the DLV approach (<xref rid="fig1" ref-type="fig">Fig. 1</xref>). Accurate identification was achieved using <italic>rpo</italic>B and <italic>mdh</italic> genes. <italic>rpo</italic>B, a protein-encoding housekeeping gene, has several potential advantages over other molecular methods. The <italic>rpo</italic>B gene occurs as a single copy in all prokaryotes, it functions as a housekeeping gene, it is less susceptible to some lateral gene transfer and its genetic divergence provides enhanced resolution for species identification. 16S rRNA gene copy number, however, varies among species and shows heterogeneity among intragenomic gene copies. <italic>rpo</italic>B is therefore the better marker to distinguish interspecies relationships between and within <italic>E. coli</italic> and <italic>Shigella</italic> spp. than 16S rRNA sequences <xref rid="bib20" ref-type="bibr">[20]</xref>. Similarly, housekeeping gene malate–lactate dehydrogenase (<italic>mdh</italic>) was reported to provide good subtype discrimination between various subspecies <xref rid="bib21" ref-type="bibr">[21]</xref>, which reveals the evolutionary histories of <italic>Salmonella</italic> and <italic>E. coli</italic> chromosomes.<fig id="fig1"><label>Fig. 1</label><caption><p>Genotypic diversification of various <italic>Escherichia coli</italic> and <italic>Shigella</italic> spp. based on highly conserved housekeeping genes <italic>mdh</italic> (A) and <italic>rpo</italic>B (B). EHEC, EIEC, EPEC, STEC and ATCC 25922 <italic>E. coli</italic> form <italic>E. coli</italic> group; <italic>S. dysenteriae, S. flexneri</italic> 2a, <italic>S. flexneri</italic> 5a, <italic>S. flexneri, S. boydii</italic> and <italic>S. sonnei</italic> from <italic>Shigella</italic> group were used to construct double-locus variant–based phylogeny. EHEC, enterohaemorrhagic <italic>E. coli</italic>; EIEC, enteroinvasive <italic>E. coli</italic>; EPEC, enteropathogenic <italic>E. coli</italic>; STEC, Shiga toxin–producing <italic>E. coli.</italic></p></caption><alt-text id="alttext0010">Fig. 1</alt-text><graphic xlink:href="gr1"></graphic></fig></p></sec><sec id="sec3.4"><title>WGS for differentiation of <italic>E. coli</italic> and <italic>Shigella</italic> spp.</title><p id="p0070">Differentiation of species based on WGS can be attained by two methods, k-mers and whole genome single nucleotide polymorphism (SNP). Chattaway <italic>et al.</italic> utilized k-mers (substrings of <italic>k</italic> nucleotides in DNA sequence data) to predict the species based on the number of co-occurring k-mers in two bacterial genomes as a measure of evolutionary relatedness. This accurately identified the strains to the species level <xref rid="bib22" ref-type="bibr">[22]</xref>, <xref rid="bib23" ref-type="bibr">[23]</xref>, <xref rid="bib24" ref-type="bibr">[24]</xref>. Among 1297 isolates, 18 were misidentified by conventional biochemicals and serotyping. Of these, 15 were intragenomic misidentifications and three were intergenomic misidentifications. These 18 isolates were then correctly identified by the k-mer approach. The phylogenetic relation of the clonal complexes derived from MLST and a minimum spanning tree confirmed that the k-mer method was accurate in discriminating <italic>Shigella</italic> spp. from <italic>E. coli.</italic></p><p id="p0075">Recently the use of whole genome SNPs for drawing phylogenetic relationships has been gaining attention. Pettengill <italic>et al.</italic><xref rid="bib25" ref-type="bibr">[25]</xref> reported the ability of SNPs to accurately identify EIEC and <italic>Shigella</italic> spp. from WGS data. This method used 404 SNP markers for differentiating <italic>Shigella</italic> and EIEC lineages. Further, Ashton <italic>et al.</italic><xref rid="bib26" ref-type="bibr">[26]</xref> proved classification of <italic>Shigella</italic> serotypes using SNPs with their evolutionary phylogenetic relationships. This seems to be an easier and more promising approach.</p></sec><sec id="sec3.5"><title>Identification based on ribosomal protein signature</title><p id="p0080">MALDI-TOF MS is used for early species-level identification. However, the power of discrimination is still considered to be low for <italic>Shigella</italic> spp. <xref rid="bib27" ref-type="bibr">[27]</xref>. In 2013, Khot and Fisher <xref rid="bib4" ref-type="bibr">[4]</xref> reported that conventional MALDI-TOF MS failed to distinguish <italic>Shigella</italic> spp. from <italic>E. coli.</italic> However, they reported that MALDI-TOF MS with an automated data analysis approach could distinguish inactive and other non-lactose-fermenting <italic>E. coli</italic> from <italic>Shigella</italic> species <xref rid="bib4" ref-type="bibr">[4]</xref>. This special approach included the use of ClinPro software's database and analysis tool functions like data preparation, model generation and spectra classification. Classification of unknown spectra for identification was achieved by using the ‘Classify’ function in ClinProTools, in which, if two or more of three spectra per isolate were assigned to the same class, the identification was accepted <xref rid="bib16" ref-type="bibr">[16]</xref>.</p><p id="p0085"><xref rid="tbl2" ref-type="table">Table 2</xref> compares the ability of each molecular method to differentiate <italic>E. coli</italic> and <italic>Shigella</italic> serogroups.<table-wrap id="tbl2" position="float"><label>Table 2</label><caption><p>List of nonmolecular and molecular methods for accurate differentiation of <italic>Escherichia coli</italic> and <italic>Shigella</italic> spp</p></caption><alt-text id="alttext0020">Table 2</alt-text><table frame="hsides" rules="groups"><thead><tr><th>Method for differentiation</th><th>Target</th><th>Level of differentiation between <italic>E. coli</italic> and <italic>Shigella</italic> spp.</th><th>References</th></tr></thead><tbody><tr><td>MALDI-TOF MS</td><td>Biomarker-based classifiers using their protein signature</td><td>Conventional MALDI-TOF MS fails to distinguish <italic>E. coli</italic> from <italic>Shigella</italic> spp. However, advanced software analytic tools like ClinPro could distinguish inactive and other non-lactose-fermenting <italic>E. coli</italic> from <italic>Shigella</italic> spp.</td><td>Francisco <italic>et al.</italic><xref rid="bib16" ref-type="bibr">[16]</xref>; Khot and Fischer <xref rid="bib4" ref-type="bibr">[4]</xref></td></tr><tr><td>Duplex real-time PCR</td><td><italic>uid</italic>A, <italic>lac</italic>Y</td><td>Method is based on target-specific real-time PCR. EIEC and <italic>Shigella</italic> spp. can be differentiated because <italic>lac</italic>Y is specific for <italic>E. coli</italic></td><td>Pavlovic <italic>et al.</italic><xref rid="bib10" ref-type="bibr">[10]</xref></td></tr><tr><td>16S rRNA sequencing</td><td>16S rRNA</td><td>Unacceptable for discrimination of <italic>E. coli</italic> and <italic>Shigella</italic> spp. because sequence similarities were >99% for EIEC, EHEC and <italic>Shigella</italic> spp.</td><td>Edwards <italic>et al.</italic><xref rid="bib12" ref-type="bibr">[12]</xref>; Chen <italic>et al.</italic><xref rid="bib13" ref-type="bibr">[13]</xref></td></tr><tr><td>MLST (conventional)</td><td>Housekeeping genes (<italic>adk, fum</italic>C, <italic>gyr</italic>B, <italic>icd, mdh, pur</italic>A, <italic>rec</italic>A)</td><td>Allele-based sequence type identification within <italic>E. coli</italic> and <italic>Shigella</italic> spp. without differentiating between them</td><td>Li <italic>et al.</italic><xref rid="bib15" ref-type="bibr">[15]</xref></td></tr><tr><td>Specific locus variants</td><td>Housekeeping genes (<italic>adk, fum</italic>C, <italic>gyr</italic>B, <italic>icd, mdh, pur</italic>A, <italic>rec</italic>A)</td><td>Uses sequence data of housekeeping genes rather than MLST allelic profiles. Can differentiate within sequence types using single-locus variant and double-locus variant approach</td><td>Gibreel <italic>et al.</italic><xref rid="bib17" ref-type="bibr">[17]</xref>; Otero <italic>et al.</italic><xref rid="bib18" ref-type="bibr">[18]</xref>; Shahsavan <italic>et al.</italic><xref rid="bib19" ref-type="bibr">[19]</xref></td></tr><tr><td>k-mer</td><td>k-mer regions</td><td>Serotype-level identification and differentiation of <italic>E. coli</italic> and <italic>Shigella</italic> spp. is performed using co-occurring k-mers</td><td>Hasman <italic>et al.</italic><xref rid="bib23" ref-type="bibr">[23]</xref>; Larsen <italic>et al.</italic><xref rid="bib24" ref-type="bibr">[24]</xref>; Chattaway <italic>et al.</italic><xref rid="bib22" ref-type="bibr">[22]</xref></td></tr><tr><td>SNP</td><td>SNP markers</td><td>Specific SNP markers were used for classification using SNPs with their evolutionary phylogenetic relationships</td><td>Ashton <italic>et al.</italic><xref rid="bib26" ref-type="bibr">[26]</xref>; Pettengill <italic>et al.</italic><xref rid="bib25" ref-type="bibr">[25]</xref></td></tr></tbody></table><table-wrap-foot><fn><p>EHEC, enterohaemorrhagic <italic>Escherichia coli</italic>; EIEC, enteroinvasive <italic>Escherichia coli</italic>; MALDI-TOF MS, matrix-assisted desorption ionization–time of flight mass spectrometry; MLST, multilocus sequence typing; SNP, single nucleotide polymorphism.</p></fn></table-wrap-foot></table-wrap></p></sec></sec><sec id="sec4"><title>Conclusion</title><p id="p0090">Among the molecular methods, we deem 16S rRNA to be unacceptable, while duplex real-time PCR and DLV using sequence data of the conserved housekeeping genes <italic>rpo</italic>B and <italic>mdh</italic> may be used. A high discriminatory potential is evident with WGS that analyses k-mers and SNPs. Among these two WGS modalities, identification using SNPs is easy to perform and analyse, and we think it is more promising. 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