Recovery of Lutacidiplasmatales archaeal order genomes suggests convergent evolution in Thermoplasmatota

Paul Sheridan; Yiyu Meng; Tom A.  Williams; Cecile Gubry-Rangin

doi:10.1038/s41467-022-31847-7

Recovery of Lutacidiplasmatales archaeal order genomes suggests convergent evolution in Thermoplasmatota

Paul Sheridan, Yiyu Meng, Tom A. Williams, Cecile Gubry-Rangin^* (Corresponding Author)

^*Corresponding author for this work

Aberdeen Centre For Environmental Sustainability

University of Bristol

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

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Abstract

The Terrestrial Miscellaneous Euryarchaeota Group has been identified in various environments, and the single genome investigated thus far suggests that these archaea are anaerobic sulfite reducers. We assemble 35 new genomes from this group that, based on genome analysis, appear to possess aerobic and facultative anaerobic lifestyles and may oxidise rather than reduce sulfite. We propose naming this order (representing 16 genera) “Lutacidiplasmatales” due to their occurrence in various acidic environments and placement within the phylum Thermoplasmatota. Phylum-level analysis reveals that Thermoplasmatota evolution had been punctuated by several periods of high levels of novel gene family acquisition. Several essential metabolisms, such as aerobic respiration and acid tolerance, were likely acquired independently by divergent lineages through convergent evolution rather than inherited from a common ancestor. Ultimately, this study describes the terrestrially prevalent Lutacidiciplasmatales and highlights convergent evolution as an important driving force in the evolution of archaeal lineages.

Original language	English
Article number	4110
Number of pages	13
Journal	Nature Communications
Volume	13
DOIs	https://doi.org/10.1038/s41467-022-31847-7
Publication status	Published - 15 Jul 2022

Bibliographical note

UKRI financially supported P.O.S. and Y.M. through the NERC grant (NE/R001529/1). In addition, C.G.-R. and T.A.W. were supported by a Royal Society University Research Fellowship (URF150571 and UF140626). We thank Tony Travis for his support with Biolinux. The authors would also like to acknowledge the support of the Maxwell computer cluster funded by the University of Aberdeen.

Data Availability Statement

Accession numbers for the 36 newly sequenced genomes presented in this study can be found in Supplementary Data 2 and under the NCBI BioProject PRJNA795910. Public data is available from NCBI (www.ncbi.nlm.nih.gov), IMG (https://img.jgi.doe.gov/), KEGG (https://www.genome.jp/kegg/), dbCAN (http://bcb.unl.edu/dbCAN2/download/), arCOG (https://ftp.ncbi.nih.gov/pub/wolf/COGs/arCOG/), PFAM (https://pfam.xfam.org/), TIGRFAM (http://tigrfams.jcvi.org/cgi-bin/index.cgi) and GTDB R202 (https://data.gtdb.ecogenomic.org/releases/). Source data are provided with this paper.

Code availability
Scripts for general manipulation of ALE outputs have been deposited at https://github.com/Tancata/phylo/tree/master/ALE (https://doi.org/10.5281/zenodo.4012549)34, and additional scripts specific to this work have been deposited at https://github.com/SheridanPO/ALE_analysis (https://doi.org/10.5281/zenodo.6598435)90.

Keywords

archaea
phylogenetics
taxonomy

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Sheridan_etal_NC_Recovery_Lutacidiplasmatales_Archael_VOR
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title = "Recovery of Lutacidiplasmatales archaeal order genomes suggests convergent evolution in Thermoplasmatota",

abstract = "The Terrestrial Miscellaneous Euryarchaeota Group has been identified in various environments, and the single genome investigated thus far suggests that these archaea are anaerobic sulfite reducers. We assemble 35 new genomes from this group that, based on genome analysis, appear to possess aerobic and facultative anaerobic lifestyles and may oxidise rather than reduce sulfite. We propose naming this order (representing 16 genera) “Lutacidiplasmatales” due to their occurrence in various acidic environments and placement within the phylum Thermoplasmatota. Phylum-level analysis reveals that Thermoplasmatota evolution had been punctuated by several periods of high levels of novel gene family acquisition. Several essential metabolisms, such as aerobic respiration and acid tolerance, were likely acquired independently by divergent lineages through convergent evolution rather than inherited from a common ancestor. Ultimately, this study describes the terrestrially prevalent Lutacidiciplasmatales and highlights convergent evolution as an important driving force in the evolution of archaeal lineages.",

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note = "UKRI financially supported P.O.S. and Y.M. through the NERC grant (NE/R001529/1). In addition, C.G.-R. and T.A.W. were supported by a Royal Society University Research Fellowship (URF150571 and UF140626). We thank Tony Travis for his support with Biolinux. The authors would also like to acknowledge the support of the Maxwell computer cluster funded by the University of Aberdeen. ",

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N2 - The Terrestrial Miscellaneous Euryarchaeota Group has been identified in various environments, and the single genome investigated thus far suggests that these archaea are anaerobic sulfite reducers. We assemble 35 new genomes from this group that, based on genome analysis, appear to possess aerobic and facultative anaerobic lifestyles and may oxidise rather than reduce sulfite. We propose naming this order (representing 16 genera) “Lutacidiplasmatales” due to their occurrence in various acidic environments and placement within the phylum Thermoplasmatota. Phylum-level analysis reveals that Thermoplasmatota evolution had been punctuated by several periods of high levels of novel gene family acquisition. Several essential metabolisms, such as aerobic respiration and acid tolerance, were likely acquired independently by divergent lineages through convergent evolution rather than inherited from a common ancestor. Ultimately, this study describes the terrestrially prevalent Lutacidiciplasmatales and highlights convergent evolution as an important driving force in the evolution of archaeal lineages.

AB - The Terrestrial Miscellaneous Euryarchaeota Group has been identified in various environments, and the single genome investigated thus far suggests that these archaea are anaerobic sulfite reducers. We assemble 35 new genomes from this group that, based on genome analysis, appear to possess aerobic and facultative anaerobic lifestyles and may oxidise rather than reduce sulfite. We propose naming this order (representing 16 genera) “Lutacidiplasmatales” due to their occurrence in various acidic environments and placement within the phylum Thermoplasmatota. Phylum-level analysis reveals that Thermoplasmatota evolution had been punctuated by several periods of high levels of novel gene family acquisition. Several essential metabolisms, such as aerobic respiration and acid tolerance, were likely acquired independently by divergent lineages through convergent evolution rather than inherited from a common ancestor. Ultimately, this study describes the terrestrially prevalent Lutacidiciplasmatales and highlights convergent evolution as an important driving force in the evolution of archaeal lineages.

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JO - Nature Communications

JF - Nature Communications

M1 - 4110

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Recovery of Lutacidiplasmatales archaeal order genomes suggests convergent evolution in Thermoplasmatota

Abstract

Bibliographical note

Data Availability Statement

Keywords

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