Phylogenetic and functional substrate specificity for endolithic microbial communities in hyper-arid environments

Under extreme water deficit, endolithic (inside rock) microbial ecosystems are considered environmental refuges for life in cold and hot deserts, yet their diversity and functional adaptations remain vastly unexplored. The metagenomic analyses of the communities from two rock substrates, calcite and...

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Autores: Crits-Christoph, Alexander, Robinson, Courtney K., Ma, Bing, Ravel, Jacques, Wierzchos, Jacek, Ascaso, Carmen, Artieda, Octavio, Souza-Egipsy, Virginia, Casero, María Cristina, DiRuggiero, Jocelyne
Tipo de recurso: artículo
Estado:Versión publicada
Fecha de publicación:2016
País:España
Institución:Consejo Superior de Investigaciones Científicas (CSIC)
Repositorio:DIGITAL.CSIC. Repositorio Institucional del CSIC
OAI Identifier:oai:digital.csic.es:10261/151462
Acceso en línea:http://hdl.handle.net/10261/151462
Access Level:acceso abierto
Palabra clave:Hyper-arid environment
Extreme environment
Metagenomics
Atacama Desert
Endoliths
Cyanobacteria
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spelling Phylogenetic and functional substrate specificity for endolithic microbial communities in hyper-arid environmentsCrits-Christoph, AlexanderRobinson, Courtney K.Ma, BingRavel, JacquesWierzchos, JacekAscaso, CarmenArtieda, OctavioSouza-Egipsy, VirginiaCasero, María CristinaDiRuggiero, JocelyneHyper-arid environmentExtreme environmentMetagenomicsAtacama DesertEndolithsCyanobacteriaUnder extreme water deficit, endolithic (inside rock) microbial ecosystems are considered environmental refuges for life in cold and hot deserts, yet their diversity and functional adaptations remain vastly unexplored. The metagenomic analyses of the communities from two rock substrates, calcite and ignimbrite, revealed that they were dominated by Cyanobacteria, Actinobacteria, and Chloroflexi. The relative distribution of major phyla was significantly different between the two substrates and biodiversity estimates, from 16S rRNA gene sequences and from the metagenomic data, all pointed to a higher taxonomic diversity in the calcite community. While both endolithic communities showed adaptations to extreme aridity and to the rock habitat, their functional capabilities revealed significant differences. ABC transporters and pathways for osmoregulation were more diverse in the calcite chasmoendolithic community. In contrast, the ignimbrite cryptoendolithic community was enriched in pathways for secondary metabolites, such as non-ribosomal peptides (NRP) and polyketides (PK). Assemblies of the metagenome data produced population genomes for the major phyla found in both communities and revealed a greater diversity of Cyanobacteria population genomes for the calcite substrate. Draft genomes of the dominant Cyanobacteria in each community were constructed with more than 93% estimated completeness. The two annotated proteomes shared 64% amino acid identity and a significantly higher number of genes involved in iron update, and NRPS gene clusters, were found in the draft genomes from the ignimbrite. Both the community-wide and genome-specific differences may be related to higher water availability and the colonization of large fissures and cracks in the calcite in contrast to a harsh competition for colonization space and nutrient resources in the narrow pores of the ignimbrite. Together, these results indicated that the habitable architecture of both lithic substrates- chasmoendolithic versus cryptoendolithic - might be an essential element in determining the colonization and the diversity of the microbial communities in endolithic substrates at the dry limit for life.ThisworkwasfundedbygrantEXOB08-0033fromNASAand grant NSF-0918907fromtheNationalSciencefoundationtoJR and byMINECO(Spain)grantsCGL2013-42509PtoJW,CA,JR, and OA.Peer ReviewedFrontiers MediaMinisterio de Economía y Competitividad (España)Consejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]2017201720162017info:eu-repo/semantics/articlehttp://purl.org/coar/resource_type/c_6501Publisher's versioninfo:eu-repo/semantics/publishedVersionhttp://hdl.handle.net/10261/151462reponame:DIGITAL.CSIC. Repositorio Institucional del CSICinstname:Consejo Superior de Investigaciones Científicas (CSIC)Inglés#PLACEHOLDER_PARENT_METADATA_VALUE#info:eu-repo/grantAgreement/MINECO/Plan Estatal de Investigación Científica y Técnica y de Innovación 2013-2016/CGL2013-42509PSíinfo:eu-repo/semantics/openAccessoai:digital.csic.es:10261/1514622026-05-22T06:33:51Z
dc.title.none.fl_str_mv Phylogenetic and functional substrate specificity for endolithic microbial communities in hyper-arid environments
title Phylogenetic and functional substrate specificity for endolithic microbial communities in hyper-arid environments
spellingShingle Phylogenetic and functional substrate specificity for endolithic microbial communities in hyper-arid environments
Crits-Christoph, Alexander
Hyper-arid environment
Extreme environment
Metagenomics
Atacama Desert
Endoliths
Cyanobacteria
title_short Phylogenetic and functional substrate specificity for endolithic microbial communities in hyper-arid environments
title_full Phylogenetic and functional substrate specificity for endolithic microbial communities in hyper-arid environments
title_fullStr Phylogenetic and functional substrate specificity for endolithic microbial communities in hyper-arid environments
title_full_unstemmed Phylogenetic and functional substrate specificity for endolithic microbial communities in hyper-arid environments
title_sort Phylogenetic and functional substrate specificity for endolithic microbial communities in hyper-arid environments
dc.creator.none.fl_str_mv Crits-Christoph, Alexander
Robinson, Courtney K.
Ma, Bing
Ravel, Jacques
Wierzchos, Jacek
Ascaso, Carmen
Artieda, Octavio
Souza-Egipsy, Virginia
Casero, María Cristina
DiRuggiero, Jocelyne
author Crits-Christoph, Alexander
author_facet Crits-Christoph, Alexander
Robinson, Courtney K.
Ma, Bing
Ravel, Jacques
Wierzchos, Jacek
Ascaso, Carmen
Artieda, Octavio
Souza-Egipsy, Virginia
Casero, María Cristina
DiRuggiero, Jocelyne
author_role author
author2 Robinson, Courtney K.
Ma, Bing
Ravel, Jacques
Wierzchos, Jacek
Ascaso, Carmen
Artieda, Octavio
Souza-Egipsy, Virginia
Casero, María Cristina
DiRuggiero, Jocelyne
author2_role author
author
author
author
author
author
author
author
author
dc.contributor.none.fl_str_mv Ministerio de Economía y Competitividad (España)
Consejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]
dc.subject.none.fl_str_mv Hyper-arid environment
Extreme environment
Metagenomics
Atacama Desert
Endoliths
Cyanobacteria
topic Hyper-arid environment
Extreme environment
Metagenomics
Atacama Desert
Endoliths
Cyanobacteria
description Under extreme water deficit, endolithic (inside rock) microbial ecosystems are considered environmental refuges for life in cold and hot deserts, yet their diversity and functional adaptations remain vastly unexplored. The metagenomic analyses of the communities from two rock substrates, calcite and ignimbrite, revealed that they were dominated by Cyanobacteria, Actinobacteria, and Chloroflexi. The relative distribution of major phyla was significantly different between the two substrates and biodiversity estimates, from 16S rRNA gene sequences and from the metagenomic data, all pointed to a higher taxonomic diversity in the calcite community. While both endolithic communities showed adaptations to extreme aridity and to the rock habitat, their functional capabilities revealed significant differences. ABC transporters and pathways for osmoregulation were more diverse in the calcite chasmoendolithic community. In contrast, the ignimbrite cryptoendolithic community was enriched in pathways for secondary metabolites, such as non-ribosomal peptides (NRP) and polyketides (PK). Assemblies of the metagenome data produced population genomes for the major phyla found in both communities and revealed a greater diversity of Cyanobacteria population genomes for the calcite substrate. Draft genomes of the dominant Cyanobacteria in each community were constructed with more than 93% estimated completeness. The two annotated proteomes shared 64% amino acid identity and a significantly higher number of genes involved in iron update, and NRPS gene clusters, were found in the draft genomes from the ignimbrite. Both the community-wide and genome-specific differences may be related to higher water availability and the colonization of large fissures and cracks in the calcite in contrast to a harsh competition for colonization space and nutrient resources in the narrow pores of the ignimbrite. Together, these results indicated that the habitable architecture of both lithic substrates- chasmoendolithic versus cryptoendolithic - might be an essential element in determining the colonization and the diversity of the microbial communities in endolithic substrates at the dry limit for life.
publishDate 2016
dc.date.none.fl_str_mv 2016
2017
2017
2017
dc.type.none.fl_str_mv info:eu-repo/semantics/article
http://purl.org/coar/resource_type/c_6501
Publisher's version
info:eu-repo/semantics/publishedVersion
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/10261/151462
url http://hdl.handle.net/10261/151462
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
dc.relation.none.fl_str_mv #PLACEHOLDER_PARENT_METADATA_VALUE#
info:eu-repo/grantAgreement/MINECO/Plan Estatal de Investigación Científica y Técnica y de Innovación 2013-2016/CGL2013-42509P
Sí
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
eu_rights_str_mv openAccess
dc.publisher.none.fl_str_mv Frontiers Media
publisher.none.fl_str_mv Frontiers Media
dc.source.none.fl_str_mv reponame:DIGITAL.CSIC. Repositorio Institucional del CSIC
instname:Consejo Superior de Investigaciones Científicas (CSIC)
instname_str Consejo Superior de Investigaciones Científicas (CSIC)
reponame_str DIGITAL.CSIC. Repositorio Institucional del CSIC
collection DIGITAL.CSIC. Repositorio Institucional del CSIC
repository.name.fl_str_mv
repository.mail.fl_str_mv
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