Gene inversion led to the emergence of brackish archaeal heterotrophs in the aftermath of the Cryogenian Snowball Earth

Fan, Lu1,2; Xu, Bu1,2; Chen, Songze2; Liu, Yang3,4; Li, Fuyan5; Xie, Wei6,7; Prabhu, Apoorva8; Zou, Dayu3,4; Wan, Ru9,10,11,12; Li, Hongliang11; Liu, Haodong1; Liu, Yuhang; Kao, Shuh-Ji9,10; Chen, Jianfang11,12; Zhu, Yuanqing1,13; Rinke, Christian; Li, Meng3,4; Zhu, Maoyan14,15,16; Zhang, Chuanlun1,2,12

2024-02-01

10.1093/pnasnexus/pgae057

PNAS NEXUS   影响因子和分区

2752-6542

Land-ocean interactions greatly impact the evolution of coastal life on earth. However, the ancient geological forces and genetic mechanisms that shaped evolutionary adaptations and allowed microorganisms to inhabit coastal brackish waters remain largely unexplored. In this study, we infer the evolutionary trajectory of the ubiquitous heterotrophic archaea Poseidoniales (Marine Group II archaea) presently occurring across global aquatic habitats. Our results show that their brackish subgroups had a single origination, dated to over 600 million years ago, through the inversion of the magnesium transport gene corA that conferred osmotic-stress tolerance. The subsequent loss and gain of corA were followed by genome-wide adjustment, characterized by a general two-step mode of selection in microbial speciation. The coastal family of Poseidoniales showed a rapid increase in the evolutionary rate during and in the aftermath of the Cryogenian Snowball Earth (similar to 700 million years ago), possibly in response to the enhanced phosphorus supply and the rise of algae. Our study highlights the close interplay between genetic changes and ecosystem evolution that boosted microbial diversification in the Neoproterozoic continental margins, where the Cambrian explosion of animals soon followed.

brackish microorganisms gene inversion archaeal evolution osmotic stress Snowball Earth

ESCI

英语

第一 ; 通讯

Science & Technology - Other Topics ; Social Sciences - Other Topics

Multidisciplinary Sciences ; Social Sciences, Interdisciplinary

WOS:001177254800010

OXFORD UNIV PRESS

Web of Science

1.Southern Univ Sci & Technol SUSTech, Dept Ocean Sci & Engn, Shenzhen Key Lab Marine Archaea Geo, Shenzhen 518055, Guangdong, Peoples R China
2.Southern Marine Sci & Engn Guangdong Lab Guangzhou, Guangzhou 511458, Guangdong, Peoples R China
3.Shenzhen Univ, Inst Adv Study, Archaeal Biol Ctr, Shenzhen 518060, Guangdong, Peoples R China
4.Shenzhen Univ, Inst Adv Study, Shenzhen Key Lab Marine Microbiome Engn, Shenzhen 518060, Guangdong, Peoples R China
5.Univ Hawaii, Daniel K Inouye Ctr Microbial Oceanog Res & Educ C, Honolulu, HI 96822 USA
6.Sun Yat Sen Univ, Sch Marine Sci, Zhuhai 519082, Guangdong, Peoples R China
7.Southern Marine Sci & Engn Guangdong Lab Zhuhai, Zhuhai 519082, Guangdong, Peoples R China
8.Univ Queensland, Australian Ctr Ecogenom, Sch Chem & Mol Biosci, Brisbane, Qld 4072, Australia
9.Hainan Univ, State Key Lab Marine Resource Utilizat South China, Haikou 570228, Hainan, Peoples R China
10.Xiamen Univ, Coll Ocean & Earth Sci, State Key Lab Marine Environm Sci, Xiamen 361005, Fujian, Peoples R China
11.Minist Nat Resources, Inst Oceanog 2, Key Lab Marine Ecosyst Dynam, Hangzhou 310012, Zhejiang, Peoples R China
12.State Key Lab Satellite Ocean Environm Dynam, Hangzhou 310012, Zhejiang, Peoples R China
13.Shanghai Earthquake Agcy, Shanghai Sheshan Natl Geophys Observ, Shanghai 200062, Peoples R China
14.Univ Chinese Acad Sci, Coll Earth & Planetary Sci, Beijing 100049, Peoples R China
15.Nanjing Inst Geol & Palaeontol, Chinese Acad Sci, State Key Lab Palaeobiol & Stratig, Nanjing 210008, Jiangsu, Peoples R China
16.Nanjing Inst Geol & Palaeontol, Chinese Acad Sci, Ctr Excellence Life & Paleoenvironment, Nanjing 210008, Jiangsu, Peoples R China

Fan, Lu,Xu, Bu,Chen, Songze,et al. Gene inversion led to the emergence of brackish archaeal heterotrophs in the aftermath of the Cryogenian Snowball Earth[J]. PNAS NEXUS,2024,3(2).

Fan, Lu.,Xu, Bu.,Chen, Songze.,Liu, Yang.,Li, Fuyan.,...&Zhang, Chuanlun.(2024).Gene inversion led to the emergence of brackish archaeal heterotrophs in the aftermath of the Cryogenian Snowball Earth.PNAS NEXUS,3(2).

Fan, Lu,et al."Gene inversion led to the emergence of brackish archaeal heterotrophs in the aftermath of the Cryogenian Snowball Earth".PNAS NEXUS 3.2(2024).