Ancestral Reconstructions Decipher Major Adaptations of Ammonia-Oxidizing Archaea upon Radiation into Moderate Terrestrial and Marine Environments

ABSTRACT Unlike all other archaeal lineages, ammonia-oxidizing archaea (AOA) of the phylum Thaumarchaeota are widespread and abundant in all moderate and oxic environments on Earth. The evolutionary adaptations that led to such unprecedented ecological success of a microbial clade characterized by h...

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Autores principales: Sophie S. Abby, Melina Kerou, Christa Schleper
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Publicado: American Society for Microbiology 2020
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spelling oai:doaj.org-article:962e9ef36dde4843a30fa5f604a0e9be2021-11-15T16:19:08ZAncestral Reconstructions Decipher Major Adaptations of Ammonia-Oxidizing Archaea upon Radiation into Moderate Terrestrial and Marine Environments10.1128/mBio.02371-202150-7511https://doaj.org/article/962e9ef36dde4843a30fa5f604a0e9be2020-10-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.02371-20https://doaj.org/toc/2150-7511ABSTRACT Unlike all other archaeal lineages, ammonia-oxidizing archaea (AOA) of the phylum Thaumarchaeota are widespread and abundant in all moderate and oxic environments on Earth. The evolutionary adaptations that led to such unprecedented ecological success of a microbial clade characterized by highly conserved energy and carbon metabolisms have, however, remained underexplored. Here, we reconstructed the genomic content and growth temperature of the ancestor of all AOA, as well as the ancestors of the marine and soil lineages, based on 39 available complete or nearly complete genomes of AOA. Our evolutionary scenario depicts an extremely thermophilic, autotrophic, aerobic ancestor from which three independent lineages of a marine and two terrestrial groups radiated into moderate environments. Their emergence was paralleled by (i) a continuous acquisition of an extensive collection of stress tolerance genes mostly involved in redox maintenance and oxygen detoxification, (ii) an expansion of regulatory capacities in transcription and central metabolic functions, and (iii) an extended repertoire of cell appendages and modifications related to adherence and interactions with the environment. Our analysis provides insights into the evolutionary transitions and key processes that enabled the conquest of the diverse environments in which contemporary AOA are found.Sophie S. AbbyMelina KerouChrista SchleperAmerican Society for Microbiologyarticletype IV pilicatalaseaconitaseArchaeaammonia oxidizing archaeareactive oxygen speciesMicrobiologyQR1-502ENmBio, Vol 11, Iss 5 (2020)
institution DOAJ
collection DOAJ
language EN
topic type IV pili
catalase
aconitase
Archaea
ammonia oxidizing archaea
reactive oxygen species
Microbiology
QR1-502
spellingShingle type IV pili
catalase
aconitase
Archaea
ammonia oxidizing archaea
reactive oxygen species
Microbiology
QR1-502
Sophie S. Abby
Melina Kerou
Christa Schleper
Ancestral Reconstructions Decipher Major Adaptations of Ammonia-Oxidizing Archaea upon Radiation into Moderate Terrestrial and Marine Environments
description ABSTRACT Unlike all other archaeal lineages, ammonia-oxidizing archaea (AOA) of the phylum Thaumarchaeota are widespread and abundant in all moderate and oxic environments on Earth. The evolutionary adaptations that led to such unprecedented ecological success of a microbial clade characterized by highly conserved energy and carbon metabolisms have, however, remained underexplored. Here, we reconstructed the genomic content and growth temperature of the ancestor of all AOA, as well as the ancestors of the marine and soil lineages, based on 39 available complete or nearly complete genomes of AOA. Our evolutionary scenario depicts an extremely thermophilic, autotrophic, aerobic ancestor from which three independent lineages of a marine and two terrestrial groups radiated into moderate environments. Their emergence was paralleled by (i) a continuous acquisition of an extensive collection of stress tolerance genes mostly involved in redox maintenance and oxygen detoxification, (ii) an expansion of regulatory capacities in transcription and central metabolic functions, and (iii) an extended repertoire of cell appendages and modifications related to adherence and interactions with the environment. Our analysis provides insights into the evolutionary transitions and key processes that enabled the conquest of the diverse environments in which contemporary AOA are found.
format article
author Sophie S. Abby
Melina Kerou
Christa Schleper
author_facet Sophie S. Abby
Melina Kerou
Christa Schleper
author_sort Sophie S. Abby
title Ancestral Reconstructions Decipher Major Adaptations of Ammonia-Oxidizing Archaea upon Radiation into Moderate Terrestrial and Marine Environments
title_short Ancestral Reconstructions Decipher Major Adaptations of Ammonia-Oxidizing Archaea upon Radiation into Moderate Terrestrial and Marine Environments
title_full Ancestral Reconstructions Decipher Major Adaptations of Ammonia-Oxidizing Archaea upon Radiation into Moderate Terrestrial and Marine Environments
title_fullStr Ancestral Reconstructions Decipher Major Adaptations of Ammonia-Oxidizing Archaea upon Radiation into Moderate Terrestrial and Marine Environments
title_full_unstemmed Ancestral Reconstructions Decipher Major Adaptations of Ammonia-Oxidizing Archaea upon Radiation into Moderate Terrestrial and Marine Environments
title_sort ancestral reconstructions decipher major adaptations of ammonia-oxidizing archaea upon radiation into moderate terrestrial and marine environments
publisher American Society for Microbiology
publishDate 2020
url https://doaj.org/article/962e9ef36dde4843a30fa5f604a0e9be
work_keys_str_mv AT sophiesabby ancestralreconstructionsdeciphermajoradaptationsofammoniaoxidizingarchaeauponradiationintomoderateterrestrialandmarineenvironments
AT melinakerou ancestralreconstructionsdeciphermajoradaptationsofammoniaoxidizingarchaeauponradiationintomoderateterrestrialandmarineenvironments
AT christaschleper ancestralreconstructionsdeciphermajoradaptationsofammoniaoxidizingarchaeauponradiationintomoderateterrestrialandmarineenvironments
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