A Combination of Extreme Environmental Conditions Favor the Prevalence of Endospore-Forming Firmicutes
Identifieur interne : 000015 ( Pmc/Curation ); précédent : 000014; suivant : 000016A Combination of Extreme Environmental Conditions Favor the Prevalence of Endospore-Forming Firmicutes
Auteurs : Sevasti Filippidou [Suisse] ; Tina Wunderlin [Suisse] ; Thomas Junier [Suisse] ; Nicole Jeanneret [Suisse] ; Cristina Dorador [Chili] ; Veronica Molina [Chili] ; David R. Johnson [Suisse] ; Pilar Junier [Suisse]Source :
- Frontiers in Microbiology [ 1664-302X ] ; 2016.
Abstract
Environmental conditions unsuitable for microbial growth are the rule rather than the exception in most habitats. In response to this, microorganisms have developed various strategies to withstand environmental conditions that limit active growth. Endospore-forming Firmicutes (EFF) deploy a myriad of survival strategies in order to resist adverse conditions. Like many bacterial groups, they can form biofilms and detect nutrient scarcity through chemotaxis. Moreover, within this paraphyletic group of Firmicutes, ecophysiological optima are diverse. Nonetheless, a response to adversity that delimits this group is the formation of wet-heat resistant spores. These strategies are energetically demanding and therefore might affect the biological success of EFF. Therefore, we hypothesize that abundance and diversity of EFF should be maximized in those environments in which the benefits of these survival strategies offsets the energetic cost. In order to address this hypothesis, geothermal and mineral springs and drillings were selected because in these environments of steep physicochemical gradients, diversified survival strategies may become a successful strategy.We collected 71 samples from geothermal and mineral environments characterized by none (null), single or multiple limiting environmental factors (temperature, pH, UV radiation, and specific mineral composition). To measure success, we quantified EFF gene copy numbers (GCN;
Url:
DOI: 10.3389/fmicb.2016.01707
PubMed: 27857706
PubMed Central: 5094177
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<front><div type="abstract" xml:lang="en"><p>Environmental conditions unsuitable for microbial growth are the rule rather than the exception in most habitats. In response to this, microorganisms have developed various strategies to withstand environmental conditions that limit active growth. Endospore-forming Firmicutes (EFF) deploy a myriad of survival strategies in order to resist adverse conditions. Like many bacterial groups, they can form biofilms and detect nutrient scarcity through chemotaxis. Moreover, within this paraphyletic group of Firmicutes, ecophysiological optima are diverse. Nonetheless, a response to adversity that delimits this group is the formation of wet-heat resistant spores. These strategies are energetically demanding and therefore might affect the biological success of EFF. Therefore, we hypothesize that abundance and diversity of EFF should be maximized in those environments in which the benefits of these survival strategies offsets the energetic cost. In order to address this hypothesis, geothermal and mineral springs and drillings were selected because in these environments of steep physicochemical gradients, diversified survival strategies may become a successful strategy.We collected 71 samples from geothermal and mineral environments characterized by none (null), single or multiple limiting environmental factors (temperature, pH, UV radiation, and specific mineral composition). To measure success, we quantified EFF gene copy numbers (GCN; <italic>spo0A</italic>
gene) in relation to total bacterial GCN (16S rRNA gene), as well as the contribution of EFF to community composition. The quantification showed that relative GCN for EFF reached up to 20% at sites characterized by multiple limiting environmental factors, whereas it corresponded to less than 1% at sites with one or no limiting environmental factor. Pyrosequencing of the 16S rRNA gene supports a higher contribution of EFF at sites with multiple limiting factors. Community composition suggested a combination of phylotypes for which active growth could be expected, and phylotypes that are most likely in the state of endospores, in all the sites. In summary, our results suggest that diversified survival strategies, including sporulation and metabolic adaptations, explain the biological success of EFF in geothermal and natural springs, and that multiple extreme environmental factors favor the prevalence of EFF.</p>
</div>
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<journal-id journal-id-type="iso-abbrev">Front Microbiol</journal-id>
<journal-id journal-id-type="publisher-id">Front. Microbiol.</journal-id>
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<issn pub-type="epub">1664-302X</issn>
<publisher><publisher-name>Frontiers Media S.A.</publisher-name>
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<article-meta><article-id pub-id-type="pmid">27857706</article-id>
<article-id pub-id-type="pmc">5094177</article-id>
<article-id pub-id-type="doi">10.3389/fmicb.2016.01707</article-id>
<article-categories><subj-group subj-group-type="heading"><subject>Microbiology</subject>
<subj-group><subject>Original Research</subject>
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</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Junier</surname>
<given-names>Thomas</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>1</sup>
</xref>
<xref ref-type="aff" rid="aff2"><sup>2</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Jeanneret</surname>
<given-names>Nicole</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>1</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Dorador</surname>
<given-names>Cristina</given-names>
</name>
<xref ref-type="aff" rid="aff3"><sup>3</sup>
</xref>
<xref ref-type="aff" rid="aff4"><sup>4</sup>
</xref>
<uri xlink:type="simple" xlink:href="http://loop.frontiersin.org/people/144520/overview"></uri>
</contrib>
<contrib contrib-type="author"><name><surname>Molina</surname>
<given-names>Veronica</given-names>
</name>
<xref ref-type="aff" rid="aff5"><sup>5</sup>
</xref>
<uri xlink:type="simple" xlink:href="http://loop.frontiersin.org/people/118157/overview"></uri>
</contrib>
<contrib contrib-type="author"><name><surname>Johnson</surname>
<given-names>David R.</given-names>
</name>
<xref ref-type="aff" rid="aff6"><sup>6</sup>
</xref>
<uri xlink:type="simple" xlink:href="http://loop.frontiersin.org/people/61135/overview"></uri>
</contrib>
<contrib contrib-type="author"><name><surname>Junier</surname>
<given-names>Pilar</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>1</sup>
</xref>
<xref ref-type="author-notes" rid="fn001"><sup>*</sup>
</xref>
<uri xlink:type="simple" xlink:href="http://loop.frontiersin.org/people/96549/overview"></uri>
</contrib>
</contrib-group>
<aff id="aff1"><sup>1</sup>
<institution>Laboratory of Microbiology, University of Neuchâtel</institution>
<country>Neuchâtel, Switzerland</country>
</aff>
<aff id="aff2"><sup>2</sup>
<institution>Vital-IT group, Swiss Institute of Bioinformatics</institution>
<country>Lausanne, Switzerland</country>
</aff>
<aff id="aff3"><sup>3</sup>
<institution>Laboratorio de Complejidad Microbiana y Ecología Funcional and Departamento de Biotecnología, Facultad de Ciencias del Mar y Recursos Biológicos, Universidad de Antofagasta</institution>
<country>Antofagasta, Chile</country>
</aff>
<aff id="aff4"><sup>4</sup>
<institution>Centre for Biotechnology and Bioengineering, CeBiB, University of Chile</institution>
<country>Santiago, Chile</country>
</aff>
<aff id="aff5"><sup>5</sup>
<institution>Departamento de Biología, Facultad de Ciencias Naturales y Exactas. Universidad de Playa Ancha</institution>
<country>Valparaíso, Chile</country>
</aff>
<aff id="aff6"><sup>6</sup>
<institution>Department of Environmental Microbiology, Swiss Federal Institute of Aquatic Science and Technology (Eawag)</institution>
<country>Dübendorf, Switzerland</country>
</aff>
<author-notes><fn fn-type="edited-by"><p>Edited by: <italic>Baolei Jia, Chung-Ang University, South Korea</italic>
</p>
</fn>
<fn fn-type="edited-by"><p>Reviewed by: <italic>Juan M. Gonzalez, Spanish National Research Council, Spain; William Thomas Self, University of Central Florida, USA; Wei-Qin Zhuang, University of Auckland, New Zealand</italic>
</p>
</fn>
<corresp id="fn001">*Correspondence: <italic>Pilar Junier, <email xlink:type="simple">pilar.junier@unine.ch</email>
</italic>
</corresp>
<fn fn-type="other" id="fn002"><p><sup>†</sup>
Present address: <italic>Tina Wunderlin, Molecular Ecology, Institute for Sustainability Science, Agroscope Zurich, Reckenholzstrasse 191, CH-8046, Zurich, Switzerland</italic>
</p>
</fn>
<fn fn-type="other" id="fn003"><p>This article was submitted to Extreme Microbiology, a section of the journal Frontiers in Microbiology</p>
</fn>
</author-notes>
<pub-date pub-type="epub"><day>03</day>
<month>11</month>
<year>2016</year>
</pub-date>
<pub-date pub-type="collection"><year>2016</year>
</pub-date>
<volume>7</volume>
<elocation-id>1707</elocation-id>
<history><date date-type="received"><day>02</day>
<month>8</month>
<year>2016</year>
</date>
<date date-type="accepted"><day>12</day>
<month>10</month>
<year>2016</year>
</date>
</history>
<permissions><copyright-statement>Copyright © 2016 Filippidou, Wunderlin, Junier, Jeanneret, Dorador, Molina, Johnson and Junier.</copyright-statement>
<copyright-year>2016</copyright-year>
<copyright-holder>Filippidou, Wunderlin, Junier, Jeanneret, Dorador, Molina, Johnson and Junier</copyright-holder>
<license xlink:href="http://creativecommons.org/licenses/by/4.0/"><license-p>This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.</license-p>
</license>
</permissions>
<abstract><p>Environmental conditions unsuitable for microbial growth are the rule rather than the exception in most habitats. In response to this, microorganisms have developed various strategies to withstand environmental conditions that limit active growth. Endospore-forming Firmicutes (EFF) deploy a myriad of survival strategies in order to resist adverse conditions. Like many bacterial groups, they can form biofilms and detect nutrient scarcity through chemotaxis. Moreover, within this paraphyletic group of Firmicutes, ecophysiological optima are diverse. Nonetheless, a response to adversity that delimits this group is the formation of wet-heat resistant spores. These strategies are energetically demanding and therefore might affect the biological success of EFF. Therefore, we hypothesize that abundance and diversity of EFF should be maximized in those environments in which the benefits of these survival strategies offsets the energetic cost. In order to address this hypothesis, geothermal and mineral springs and drillings were selected because in these environments of steep physicochemical gradients, diversified survival strategies may become a successful strategy.We collected 71 samples from geothermal and mineral environments characterized by none (null), single or multiple limiting environmental factors (temperature, pH, UV radiation, and specific mineral composition). To measure success, we quantified EFF gene copy numbers (GCN; <italic>spo0A</italic>
gene) in relation to total bacterial GCN (16S rRNA gene), as well as the contribution of EFF to community composition. The quantification showed that relative GCN for EFF reached up to 20% at sites characterized by multiple limiting environmental factors, whereas it corresponded to less than 1% at sites with one or no limiting environmental factor. Pyrosequencing of the 16S rRNA gene supports a higher contribution of EFF at sites with multiple limiting factors. Community composition suggested a combination of phylotypes for which active growth could be expected, and phylotypes that are most likely in the state of endospores, in all the sites. In summary, our results suggest that diversified survival strategies, including sporulation and metabolic adaptations, explain the biological success of EFF in geothermal and natural springs, and that multiple extreme environmental factors favor the prevalence of EFF.</p>
</abstract>
<kwd-group><kwd>endospores</kwd>
<kwd>Firmicutes</kwd>
<kwd>qPCR</kwd>
<kwd>spo0A</kwd>
<kwd>16S rRNA gene</kwd>
<kwd><italic>Clostridium</italic>
</kwd>
<kwd>geothermal springs</kwd>
<kwd>mineral springs</kwd>
</kwd-group>
<funding-group><award-group><funding-source id="cn001">Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung<named-content content-type="fundref-id">10.13039/501100001711</named-content>
</funding-source>
<award-id rid="cn001">31003A_132358/1, 31003A_152972</award-id>
</award-group>
</funding-group>
<counts><fig-count count="3"></fig-count>
<table-count count="1"></table-count>
<equation-count count="0"></equation-count>
<ref-count count="74"></ref-count>
<page-count count="11"></page-count>
<word-count count="0"></word-count>
</counts>
</article-meta>
</front>
</pmc>
</record>
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