Genomic inference of the metabolism and evolution of the archaeal phylum Aigarchaeota

Zheng Shuang Hua; Yan Ni Qu; Qiyun Zhu; En Min Zhou; Yan Ling Qi; Yi Rui Yin; Yang Zhi Rao; Ye Tian; Yu Xian Li; Lan Liu; Cindy J. Castelle; Brian P. Hedlund; Wen Sheng Shu; Rob Knight; Wen Jun Li

doi:10.1038/s41467-018-05284-4

Genomic inference of the metabolism and evolution of the archaeal phylum Aigarchaeota

Zheng Shuang Hua, Yan Ni Qu, Qiyun Zhu, En Min Zhou, Yan Ling Qi, Yi Rui Yin, Yang Zhi Rao, Ye Tian, Yu Xian Li, Lan Liu, Cindy J. Castelle, Brian P. Hedlund, Wen Sheng Shu, Rob Knight, Wen Jun Li

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

35 Scopus citations

Abstract

Microbes of the phylum Aigarchaeota are widely distributed in geothermal environments, but their physiological and ecological roles are poorly understood. Here we analyze six Aigarchaeota metagenomic bins from two circumneutral hot springs in Tengchong, China, to reveal that they are either strict or facultative anaerobes, and most are chemolithotrophs that can perform sulfide oxidation. Applying comparative genomics to the Thaumarchaeota and Aigarchaeota, we find that they both originated from thermal habitats, sharing 1154 genes with their common ancestor. Horizontal gene transfer played a crucial role in shaping genetic diversity of Aigarchaeota and led to functional partitioning and ecological divergence among sympatric microbes, as several key functional innovations were endowed by Bacteria, including dissimilatory sulfite reduction and possibly carbon monoxide oxidation. Our study expands our knowledge of the possible ecological roles of the Aigarchaeota and clarifies their evolutionary relationship to their sister lineage Thaumarchaeota.

Original language	English (US)
Article number	2832
Journal	Nature communications
Volume	9
Issue number	1
DOIs	https://doi.org/10.1038/s41467-018-05284-4
State	Published - Dec 1 2018
Externally published	Yes

ASJC Scopus subject areas

Chemistry(all)
Biochemistry, Genetics and Molecular Biology(all)
Physics and Astronomy(all)

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10.1038/s41467-018-05284-4

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Genomic inference of the metabolism and evolution of the archaeal phylum Aigarchaeota. / Hua, Zheng Shuang; Qu, Yan Ni; Zhu, Qiyun; Zhou, En Min; Qi, Yan Ling; Yin, Yi Rui; Rao, Yang Zhi; Tian, Ye; Li, Yu Xian; Liu, Lan; Castelle, Cindy J.; Hedlund, Brian P.; Shu, Wen Sheng; Knight, Rob; Li, Wen Jun.

In: Nature communications, Vol. 9, No. 1, 2832, 01.12.2018.

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

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title = "Genomic inference of the metabolism and evolution of the archaeal phylum Aigarchaeota",

abstract = "Microbes of the phylum Aigarchaeota are widely distributed in geothermal environments, but their physiological and ecological roles are poorly understood. Here we analyze six Aigarchaeota metagenomic bins from two circumneutral hot springs in Tengchong, China, to reveal that they are either strict or facultative anaerobes, and most are chemolithotrophs that can perform sulfide oxidation. Applying comparative genomics to the Thaumarchaeota and Aigarchaeota, we find that they both originated from thermal habitats, sharing 1154 genes with their common ancestor. Horizontal gene transfer played a crucial role in shaping genetic diversity of Aigarchaeota and led to functional partitioning and ecological divergence among sympatric microbes, as several key functional innovations were endowed by Bacteria, including dissimilatory sulfite reduction and possibly carbon monoxide oxidation. Our study expands our knowledge of the possible ecological roles of the Aigarchaeota and clarifies their evolutionary relationship to their sister lineage Thaumarchaeota.",

author = "Hua, {Zheng Shuang} and Qu, {Yan Ni} and Qiyun Zhu and Zhou, {En Min} and Qi, {Yan Ling} and Yin, {Yi Rui} and Rao, {Yang Zhi} and Ye Tian and Li, {Yu Xian} and Lan Liu and Castelle, {Cindy J.} and Hedlund, {Brian P.} and Shu, {Wen Sheng} and Rob Knight and Li, {Wen Jun}",

note = "Funding Information: We thank the Guangdong Magigene Biotechnology Co., Ltd. China for the assistance in data analysis, and the entire staff from Yunnan Tengchong Volcano and Spa Tourist Attraction Development Corporation for strong support. This work was financially supported by the Key Project of International Cooperation of China Ministry of Science and Technology (No. 2013DFA31980), Science and Technology Infrastructure work project of China Ministry of Science and Technology (No. 2015FY110100), the National Natural Science Foundation of China (31600298, U1201233, 31470139 and 31370154), Natural Science Foundation of Guangdong Province, China (No. 2016A030312003), the China Postdoctoral Science Foundation (2016M602567), the Guangdong Province Key Laboratory of Computational Science and the Guangdong Province Computational Science Innovative Research Team. W.J.L. was also supported by Guangdong Province Higher Vocational Colleges and Schools Pearl River Scholar Funded Scheme (2014). Publisher Copyright: {\textcopyright} 2018, The Author(s).",

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AU - Qu, Yan Ni

AU - Zhu, Qiyun

AU - Zhou, En Min

AU - Qi, Yan Ling

AU - Yin, Yi Rui

AU - Rao, Yang Zhi

AU - Tian, Ye

AU - Li, Yu Xian

AU - Liu, Lan

AU - Castelle, Cindy J.

AU - Hedlund, Brian P.

AU - Shu, Wen Sheng

AU - Knight, Rob

AU - Li, Wen Jun

N1 - Funding Information: We thank the Guangdong Magigene Biotechnology Co., Ltd. China for the assistance in data analysis, and the entire staff from Yunnan Tengchong Volcano and Spa Tourist Attraction Development Corporation for strong support. This work was financially supported by the Key Project of International Cooperation of China Ministry of Science and Technology (No. 2013DFA31980), Science and Technology Infrastructure work project of China Ministry of Science and Technology (No. 2015FY110100), the National Natural Science Foundation of China (31600298, U1201233, 31470139 and 31370154), Natural Science Foundation of Guangdong Province, China (No. 2016A030312003), the China Postdoctoral Science Foundation (2016M602567), the Guangdong Province Key Laboratory of Computational Science and the Guangdong Province Computational Science Innovative Research Team. W.J.L. was also supported by Guangdong Province Higher Vocational Colleges and Schools Pearl River Scholar Funded Scheme (2014). Publisher Copyright: © 2018, The Author(s).

PY - 2018/12/1

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N2 - Microbes of the phylum Aigarchaeota are widely distributed in geothermal environments, but their physiological and ecological roles are poorly understood. Here we analyze six Aigarchaeota metagenomic bins from two circumneutral hot springs in Tengchong, China, to reveal that they are either strict or facultative anaerobes, and most are chemolithotrophs that can perform sulfide oxidation. Applying comparative genomics to the Thaumarchaeota and Aigarchaeota, we find that they both originated from thermal habitats, sharing 1154 genes with their common ancestor. Horizontal gene transfer played a crucial role in shaping genetic diversity of Aigarchaeota and led to functional partitioning and ecological divergence among sympatric microbes, as several key functional innovations were endowed by Bacteria, including dissimilatory sulfite reduction and possibly carbon monoxide oxidation. Our study expands our knowledge of the possible ecological roles of the Aigarchaeota and clarifies their evolutionary relationship to their sister lineage Thaumarchaeota.

AB - Microbes of the phylum Aigarchaeota are widely distributed in geothermal environments, but their physiological and ecological roles are poorly understood. Here we analyze six Aigarchaeota metagenomic bins from two circumneutral hot springs in Tengchong, China, to reveal that they are either strict or facultative anaerobes, and most are chemolithotrophs that can perform sulfide oxidation. Applying comparative genomics to the Thaumarchaeota and Aigarchaeota, we find that they both originated from thermal habitats, sharing 1154 genes with their common ancestor. Horizontal gene transfer played a crucial role in shaping genetic diversity of Aigarchaeota and led to functional partitioning and ecological divergence among sympatric microbes, as several key functional innovations were endowed by Bacteria, including dissimilatory sulfite reduction and possibly carbon monoxide oxidation. Our study expands our knowledge of the possible ecological roles of the Aigarchaeota and clarifies their evolutionary relationship to their sister lineage Thaumarchaeota.

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Genomic inference of the metabolism and evolution of the archaeal phylum Aigarchaeota

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