Gene duplication drives genome expansion in a major lineage of Thaumarchaeota

Paul Sheridan; Sebastien Raguideau; Christopher Quince; Jennifer Holden; Lihong  Zhang; Thames Consortium; Tom A.  Williams; Cecile Gubry-Rangin

doi:10.1038/s41467-020-19132-x

Gene duplication drives genome expansion in a major lineage of Thaumarchaeota

Paul Sheridan, Sebastien Raguideau, Christopher Quince, Jennifer Holden, Lihong Zhang, Thames Consortium, Tom A. Williams, Cecile Gubry-Rangin^* (Corresponding Author)

^*Corresponding author for this work

Aberdeen Centre For Environmental Sustainability

Newcastle University

Research output: Contribution to journal › Article › peer-review

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Abstract

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.

Original language	English
Article number	5494
Number of pages	12
Journal	Nature Communications
Volume	11
Early online date	30 Oct 2020
DOIs	https://doi.org/10.1038/s41467-020-19132-x
Publication status	Published - 30 Oct 2020

Bibliographical note

Acknowledgements
This work and P.O.S. were financially supported by UKRI through the NERC grant NE/R001529/1. In addition, C.G.-R. and T.A.W. were both supported by a Royal Society University Research Fellowship (URF150571 and UF140626). C.Q. was funded through an MRC fellowship (MR/M50161X/1) as part of the CLoud Infrastructure for Microbial Genomics (CLIMB) consortium (MR/L015080/1). S.R. was funded through the BBSRC grant BB/R015171/1. The Thames Metagenome Database was funded through the NERC grants NE/M011674/1, NE/M011259/1 and NE/M01133X/1. We thank Dr Tony Travis for his support with Biolinux and acknowledge Prof Jim Prosser for his critical reading of the manuscript. The authors would also like to acknowledge the support of the Maxwell computer cluster funded by the University of Aberdeen.

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Cite this

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abstract = "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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AU - Gubry-Rangin, Cecile

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Gene duplication drives genome expansion in a major lineage of Thaumarchaeota

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Gene duplication drives genome expansion in a major lineage of Thaumarchaeota

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