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Determinants of the adaptation of endospore-forming bacteria to extreme environments

English title Determinants of the adaptation of endospore-forming bacteria to extreme environments
Applicant Junier Pilar Eugenia
Number 152972
Funding scheme Project funding
Research institution Laboratoire de Microbiologie Institut de Biologie Université de Neuchâtel
Institution of higher education University of Neuchatel - NE
Main discipline Experimental Microbiology
Start/End 01.05.2014 - 31.05.2016
Approved amount 350'000.00
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All Disciplines (4)

Discipline
Experimental Microbiology
Molecular Biology
Genetics
Environmental Research

Keywords (5)

Endospores; Extremophiles; Geothermal activity; Genomics ; Heavy and trace metal tolerance

Lay Summary (French)

Lead
Les bactéries endosporulantes (BES) sont un groupe de bactéries capables de former des structures de survie appelées “endospores” adaptées aux stress environnementaux. Le but de ce projet est donc d'étendre nos connaissances des causes de ces adaptations.
Lay summary

Contexte

Les bactéries endosporulantes (BES) sont un groupe de bactéries capables de former des structures de survie appelées “endospores”. On les considérait jusqu'ici comme un des groupes bactériens les mieux étudiés. Cette opinion était toutefois basée sur des cultures de BES en laboratoire. Or, au cours du projet SNF "Metabolic capabilities of spore-forming bacteria" (FN31003A-132358), nous avons montré que les connaissances fondées sur les cultures sont lacunaires. Nous avons identifié des gènes qui nous ont permis d'étudier ces bactéries sans passer par une étape de culture - directement à partir d'échantillons environnementaux - par exemple pour l'étude des liens de parenté au sein des communautés de BES, ou pour le recensement de ces bactéries dans les communautés microbiennes complexes. Nous avons ainsi démontré un lien entre les BES et des menaces environnementales comme les métaux lourds dans les sédiments. Nous avons aussi mené un suivi global de l'abondance des BES vivant dans des conditions extrêmes de salinité, de rayonnement UV, de sécheresse et de température. Ce suivi global montre que les BES sont effectivement favorisées dans ces environnements extrêmes. Nous avons aussi identifé près de 190 souches, dont plusieurs d'entre elles présentent une résistance naturelle à ces conditions extrêmes. 

Buts

Ces résultats suggèrent que les BES sont adaptées aux stress environnementaux. Le but de ce projet est donc d'étendre nos connaissances des causes de ces adaptations. Nous proposons d'aborder les questions suivantes: Par quells mécanismes les bactéries endosporulantes résistent-elles aux métaux lourds ? Comment s'adaptent-elles aux environnements pauvres en nutriments ? Le résultat escompté de ce projet est la découverte d'une part de nouveaux genes ou protéines impliqués dans ces mécanismes de résistance - si possible avec des applications biotechnologiques - et d'autre part de voies métaboliques entières, non encore décrites chez ce groupe de bactéries.

Direct link to Lay Summary Last update: 02.04.2014

Responsible applicant and co-applicants

Employees

Publications

Publication
A Combination of Extreme Environmental Conditions Favor the Prevalence of Endospore-Forming Firmicutes
Filippidou Sevasti, Wunderlin Tina, Junier Thomas, Jeanneret Nicole, Dorador Cristina, Molina Veronica, Johnson David R., Junier Pilar (2016), A Combination of Extreme Environmental Conditions Favor the Prevalence of Endospore-Forming Firmicutes, in Frontiers in Microbiology, 7, 1707.
Description of Anoxybacillus geothermalis sp. nov., an aerobic endospore-forming bacterium isolated from mineral deposits in the Groß Schönebeck geothermal station, Germany
Filippidou Sevasti, Jaussi Marion, Junier Thomas, Wunderlin Tina, Jeanneret Nicole, Palmieri Fabio, Palmieri Ilona, Roussel-Delif Ludovic, Vieth-Hillebrand Andrea, Vetter Alexandra, Chain Patrick S., Regenspurg Simona, Junier Pilar (2016), Description of Anoxybacillus geothermalis sp. nov., an aerobic endospore-forming bacterium isolated from mineral deposits in the Groß Schönebeck geothermal station, Germany, in International Journal of Systematic and Evolutionary Microbiology, 66, 2944-2951.
Effect of organic carbon and metal accumulation on the bacterial communities in sulphidogenic sediments
Matthieu Bueche, Junier Pilar (2016), Effect of organic carbon and metal accumulation on the bacterial communities in sulphidogenic sediments, in Environmental Science and Pollution Research, 23(11), 10443-10456.
Manganese-II oxidation and Copper-II resistance in endospore forming Firmicutes isolated from uncontaminated environmental sites
Ganesan Sathiyanarayanan, Filippidou Sevasti, Junier Thomas, Muñoz-Rufatt Patricio, Jeanneret Nicole, Wunderlin Tina, Sieber Nathalie, Dorador Cristina, Junier Pilar (2016), Manganese-II oxidation and Copper-II resistance in endospore forming Firmicutes isolated from uncontaminated environmental sites, in AIMS Environmental Science, 3(2), 220-238.
Physical isolation of endospores from environmental samples by targeted lysis of vegetative cells
Wunderlin Tina, Junier Thomas, Paul Christophe, Jeanneret Nicole, Junier Pilar (2016), Physical isolation of endospores from environmental samples by targeted lysis of vegetative cells, in Journal of Visual Experiments, 107, e53411.
Genome Sequence of Aeribacillus pallidus Strain GS3372, an Endospore-Forming Bacterium Isolated in a Deep Geothermal Reservoir.
Filippidou Sevasti, Jaussi Marion, Junier Thomas, Wunderlin Tina, Jeanneret Nicole, Regenspurg Simona, Li Po-E, Lo Chien-Chi, Johnson Shannon, McMurry Kim, Gleasner Cheryl D, Vuyisich Momchilo, Chain Patrick S, Junier Pilar (2015), Genome Sequence of Aeribacillus pallidus Strain GS3372, an Endospore-Forming Bacterium Isolated in a Deep Geothermal Reservoir., in Genome announcements, 3(4), e00982-15.
Genome Sequence of Anoxybacillus geothermalis Strain GSsed3, a Novel Thermophilic Endospore-Forming Species.
Filippidou Sevasti, Jaussi Marion, Junier Thomas, Wunderlin Tina, Roussel-Delif Ludovic, Jeanneret Nicole, Vieth-Hillebrand Andrea, Vetter Alexandra, Regenspurg Simona, Johnson Shannon L, McMurry Kim, Gleasner Cheryl D, Lo Chien-Chi, Li Paul, Vuyisich Momchilo, Chain Patrick S, Junier Pilar (2015), Genome Sequence of Anoxybacillus geothermalis Strain GSsed3, a Novel Thermophilic Endospore-Forming Species., in Genome announcements, 3(3), e00575-15.
Genome Sequence of Bacillus alveayuensis Strain 24KAM51, a Halotolerant Thermophile Isolated from a Hydrothermal Vent.
Filippidou Sevasti, Wunderlin Tina, Junier Thomas, Jeanneret Nicole, Johnson Shannon, McMurry Kim, Gleasner Cheryl D, Lo Chien-Chi, Li Po-E, Vuyisich Momchilo, Chain Patrick S, Junier Pilar (2015), Genome Sequence of Bacillus alveayuensis Strain 24KAM51, a Halotolerant Thermophile Isolated from a Hydrothermal Vent., in Genome announcements, 3(4), e00981-15.
Genome Sequence of Kosakonia radicincitans Strain YD4, a Plant Growth-Promoting Rhizobacterium Isolated from Yerba Mate (Ilex paraguariensis St. Hill.).
Bergottini Veronica M, Filippidou Sevasti, Junier Thomas, Johnson Shannon, Chain Patrick S, Otegui Monica B, Zapata Pedro D, Junier Pilar (2015), Genome Sequence of Kosakonia radicincitans Strain YD4, a Plant Growth-Promoting Rhizobacterium Isolated from Yerba Mate (Ilex paraguariensis St. Hill.)., in Genome announcements, 3(2), e00239-15.
MLgsc: A Maximum-Likelihood General Sequence Classifier.
Junier Thomas, Hervé Vincent, Wunderlin Tina, Junier Pilar (2015), MLgsc: A Maximum-Likelihood General Sequence Classifier., in PloS one, 10(7), 0129384-0129384.
Under-detection of endospore-forming Firmicutes in metagenomic data.
Filippidou Sevasti, Junier Thomas, Wunderlin Tina, Lo Chien-Chi, Li Po-E, Chain Patrick S, Junier Pilar (2015), Under-detection of endospore-forming Firmicutes in metagenomic data., in Computational and structural biotechnology journal, 13, 299-306.

Collaboration

Group / person Country
Types of collaboration
Los Alamos National Laboratory United States of America (North America)
- in-depth/constructive exchanges on approaches, methods or results
- Publication
- Research Infrastructure
Analytical and Environmental Chemistry, University of Geneva Switzerland (Europe)
- in-depth/constructive exchanges on approaches, methods or results
- Publication
- Research Infrastructure
Department of Aquaculture, University of Antofagasta Chile (South America)
- in-depth/constructive exchanges on approaches, methods or results
- Publication
- Exchange of personnel
International Center for Geothermal Research, GFZ Germany (Europe)
- in-depth/constructive exchanges on approaches, methods or results
- Publication

Scientific events

Active participation

Title Type of contribution Title of article or contribution Date Place Persons involved
6th Swiss Microbial Ecology Meeting Poster Emergent spatial patterns allow the coexistence of competing bacterial species in a homogeneous environment 10.09.2015 Ascona, Switzerland Filippidou Sevasti; Junier Pilar Eugenia;
Second EMBO Conference on Aquatic Microbial Ecology (SAME-14) Poster New insights in the bioremediation of metals in runoff water 23.08.2015 Uppsala, Sweden Junier Pilar Eugenia; Bueche Matthieu;
72nd Annual Assembly of the Swiss Society for Microbiology Poster Breaking Bacterial Stereotypes: The Case of a Spore-Former Member of a Non-sporulating Genus 19.06.2015 Fribourg, Switzerland Junier Thomas; Junier Pilar Eugenia; Filippidou Sevasti;
6th Congress of European Microbiologists Poster When microbial survival strategies never stop to wonder: sporulation outside Firmicutes 07.06.2015 Maastricht, Netherlands Junier Pilar Eugenia; Filippidou Sevasti; Bueche Matthieu; Junier Thomas;
6th Congress of European Microbiologists (FEMS 2015) Talk given at a conference Use of Endospore-Forming Firmicutes for the bioremediation of trace-metals 07.06.2015 Maastricht, Netherlands Junier Pilar Eugenia; Bueche Matthieu;
73rd Annual Assembly of the Swiss Society for Microbiology Talk given at a conference Sporulation in Serratia ureilytica : The discovery of a novel sporulation pathway 28.05.2015 Lugano, Switzerland Bueche Matthieu; Junier Pilar Eugenia; Filippidou Sevasti; Junier Thomas;
5th International Multidisciplinary Conference on Hydrology and Ecology (HydroEco 2015) Poster New insights in the bioremediation of metals in runoff water 13.04.2015 Vienna, Austria Junier Pilar Eugenia; Bueche Matthieu;
Partec Users’ meeting 2014 Talk given at a conference Total bacterial and endospore count in sediment of Lake Cadagno (Ti) 05.11.2014 Olten, Switzerland Junier Pilar Eugenia; Bueche Matthieu;
15th International Symposium on Microbial Ecology Talk given at a conference Survival strategy meets classic ecological theories: the case of endospore-forming bacteria diversity and abundance in extreme environments 24.08.2014 Seoul, Korean Republic (South Korea) Filippidou Sevasti; Junier Pilar Eugenia; Junier Thomas;
72th meeting of the Swiss Society for Microbiology (SGM/SSM) Poster Endosporulation as a survival strategy in metal contaminated sediments 19.06.2014 Fribourg, Switzerland Bueche Matthieu; Junier Pilar Eugenia; Junier Thomas;


Awards

Title Year
Best poster presentation. 72nd Annual Assembly of the Swiss Society for Microbiology. 2014

Associated projects

Number Title Start Funding scheme
132358 Metabolic capabilities of spore-forming microorganisms 01.10.2010 Project funding

Abstract

Endospore-forming bacteria (EFB) are a paraphyletic group of Gram-positive bacteria belonging to the phylum Firmicutes. Some are well known as human pathogens (e.g. Bacilllus anthracis or Clostridium botulinum), but much less studied from an ecological point of view. Until now, and based mainly on culturing, EFB were considered one of the best-characterized microbial groups (over 90 representative genera). However during the SNF project “Metabolic capabilities of spore-forming bacteria” (FN 31003A-132358) we have developed methodological approaches that have shown that this group is currently overlooked by culture-independent approaches. We have identified genetic markers that can be used to study EFB directly from environmental samples without cultivation. In particular the gene encoding for the master regulator of the genetic cascade leading to the formation of endospores (spo0A) has shown to be present in all and is exclusive to EFB. This gene was used to develop culture-independent approaches for the phylogenetic assessment of EFB communities, as well for the quantification of EFB in complex microbial communities. These methods have been applied to evaluate our overall hypothesis that endospore formation is a survival strategy favored in extreme environments. In this context we have shown for the first time a correlation of EFB and environmental hazards such as elevated heavy and trace metals (HTM) content in sediments and lake eutrophication. We have also carried out a global survey of EFB prevalence (relative to total bacteria) for environments with high salt content, exposed to UV radiation and desiccation, as well as natural and manmade geothermal sites (specific range of electron donors/acceptors, temperature and pH conditions). This global survey indicates that EFB are indeed favored under extreme environmental conditions. The molecular study has been complemented by an effort to culture and characterize new EFB strains. We have identified close to 190 strains and several of those present a natural resistance to stress, including the tolerance to copper and manganese, as well as salinity and acidic pH.In summary all our preliminary results suggest that EFB are adapted to stress factors and therefore the aim of this project is to advance in our understanding of the determinants (genetic and physiological) for these adaptations. For this we propose to combine various approaches including comparative genomics, expression analysis, single-cell genomics, metagenomics, and experimental validation to answer the following specific questions: are EFB favored in other HTM-impacted environments? What are the mechanisms of HTM tolerance and immobilization found in EFB? What are the specific adaptations of EFB to oligotrophic environments? The expected outcome of this project is on the one hand to discover new genes/proteins involved in HTM tolerance that can have a biotechnological application, and on the other to discover entire new metabolic pathways never reported for this bacterial group.
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