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Gene duplication drives genome expansion in a major lineage of Thaumarchaeota

Ammonia-oxidising archaea of the phylum Thaumarchaeota are important organisms in the nitrogen cycle, but the mechanisms driving their radiation into diverse ecosystems remain underexplored. Here, existing thaumarchaeotal genomes are complemented with 12 genomes belonging to the previously under-sam...

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Autores principales: Sheridan, Paul O., Raguideau, Sebastien, Quince, Christopher, Holden, Jennifer, Zhang, Lihong, Williams, Tom A., Gubry-Rangin, Cécile
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7603488/
https://www.ncbi.nlm.nih.gov/pubmed/33127895
http://dx.doi.org/10.1038/s41467-020-19132-x
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author Sheridan, Paul O.
Raguideau, Sebastien
Quince, Christopher
Holden, Jennifer
Zhang, Lihong
Williams, Tom A.
Gubry-Rangin, Cécile
author_facet Sheridan, Paul O.
Raguideau, Sebastien
Quince, Christopher
Holden, Jennifer
Zhang, Lihong
Williams, Tom A.
Gubry-Rangin, Cécile
author_sort Sheridan, Paul O.
collection PubMed
description Ammonia-oxidising archaea of the phylum Thaumarchaeota are important organisms in the nitrogen cycle, but the mechanisms driving their radiation into diverse ecosystems remain underexplored. Here, existing thaumarchaeotal genomes are complemented with 12 genomes belonging to the previously under-sampled Nitrososphaerales to investigate the impact of lateral gene transfer (LGT), gene duplication and loss across thaumarchaeotal evolution. We reveal a major role for gene duplication in driving genome expansion subsequent to early LGT. In particular, two large LGT events are identified into Nitrososphaerales and the fate of these gene families is highly lineage-specific, being lost in some descendant lineages, but undergoing extensive duplication in others, suggesting niche-specific roles. Notably, some genes involved in carbohydrate transport or coenzyme metabolism were duplicated, likely facilitating niche specialisation in soils and sediments. Overall, our results suggest that LGT followed by gene duplication drives Nitrososphaerales evolution, highlighting a previously under-appreciated mechanism of genome expansion in archaea.
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spelling pubmed-76034882020-11-10 Gene duplication drives genome expansion in a major lineage of Thaumarchaeota Sheridan, Paul O. Raguideau, Sebastien Quince, Christopher Holden, Jennifer Zhang, Lihong Williams, Tom A. Gubry-Rangin, Cécile Nat Commun Article Ammonia-oxidising archaea of the phylum Thaumarchaeota are important organisms in the nitrogen cycle, but the mechanisms driving their radiation into diverse ecosystems remain underexplored. Here, existing thaumarchaeotal genomes are complemented with 12 genomes belonging to the previously under-sampled Nitrososphaerales to investigate the impact of lateral gene transfer (LGT), gene duplication and loss across thaumarchaeotal evolution. We reveal a major role for gene duplication in driving genome expansion subsequent to early LGT. In particular, two large LGT events are identified into Nitrososphaerales and the fate of these gene families is highly lineage-specific, being lost in some descendant lineages, but undergoing extensive duplication in others, suggesting niche-specific roles. Notably, some genes involved in carbohydrate transport or coenzyme metabolism were duplicated, likely facilitating niche specialisation in soils and sediments. Overall, our results suggest that LGT followed by gene duplication drives Nitrososphaerales evolution, highlighting a previously under-appreciated mechanism of genome expansion in archaea. Nature Publishing Group UK 2020-10-30 /pmc/articles/PMC7603488/ /pubmed/33127895 http://dx.doi.org/10.1038/s41467-020-19132-x Text en © The Author(s) 2020 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.
spellingShingle Article
Sheridan, Paul O.
Raguideau, Sebastien
Quince, Christopher
Holden, Jennifer
Zhang, Lihong
Williams, Tom A.
Gubry-Rangin, Cécile
Gene duplication drives genome expansion in a major lineage of Thaumarchaeota
title Gene duplication drives genome expansion in a major lineage of Thaumarchaeota
title_full Gene duplication drives genome expansion in a major lineage of Thaumarchaeota
title_fullStr Gene duplication drives genome expansion in a major lineage of Thaumarchaeota
title_full_unstemmed Gene duplication drives genome expansion in a major lineage of Thaumarchaeota
title_short Gene duplication drives genome expansion in a major lineage of Thaumarchaeota
title_sort gene duplication drives genome expansion in a major lineage of thaumarchaeota
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7603488/
https://www.ncbi.nlm.nih.gov/pubmed/33127895
http://dx.doi.org/10.1038/s41467-020-19132-x
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