Novel order-level lineage of ammonia-oxidizing archaea widespread in marine and terrestrial environments

Zheng, Yue1; Wang, Baozhan2; Gao, Ping2; Yang, Yiyan3; Xu, Bu4,5; Su, Xiaoquan6; Ning, Daliang7; Tao, Qing7; Li, Qian8; Zhao, Feng9; Wang, Dazhi; Zhang, Yao8; Li, Meng10; Winkler, Mari-K H.11; Ingalls, Anitra E.12; Zhou, Jizhong13,14; Zhang, Chuanlun4,5; Stahl, David A.11; Jiang, Jiandong2,7; Martens-Habbena, Willm15; Qin, Wei7

2024-01-08

10.1093/ismejo/wrad002

ISME JOURNAL   影响因子和分区

1751-7362

1751-7370

Ammonia-oxidizing archaea (AOA) are among the most ubiquitous and abundant archaea on Earth, widely distributed in marine, terrestrial, and geothermal ecosystems. However, the genomic diversity, biogeography, and evolutionary process of AOA populations in subsurface environments are vastly understudied compared to those in marine and soil systems. Here, we report a novel AOA order Candidatus (Ca.) Nitrosomirales which forms a sister lineage to the thermophilic Ca. Nitrosocaldales. Metagenomic and 16S rRNA gene-read mapping demonstrates the abundant presence of Nitrosomirales AOA in various groundwater environments and their widespread distribution across a range of geothermal, terrestrial, and marine habitats. Terrestrial Nitrosomirales AOA show the genetic capacity of using formate as a source of reductant and using nitrate as an alternative electron acceptor. Nitrosomirales AOA appear to have acquired key metabolic genes and operons from other mesophilic populations via horizontal gene transfer, including genes encoding urease, nitrite reductase, and V-type ATPase. The additional metabolic versatility conferred by acquired functions may have facilitated their radiation into a variety of subsurface, marine, and soil environments. We also provide evidence that each of the four AOA orders spans both marine and terrestrial habitats, which suggests a more complex evolutionary history for major AOA lineages than previously proposed. Together, these findings establish a robust phylogenomic framework of AOA and provide new insights into the ecology and adaptation of this globally abundant functional guild.

Nitrosomirales ammonia-oxidizing archaea nitrification subsurface sponge formate metabolism nitrate reduction

SCI

英语

其他

Environmental Sciences & Ecology ; Microbiology

Ecology ; Microbiology

WOS:001166842600011

OXFORD UNIV PRESS

Web of Science

1.Xiamen Univ, Coll Environm & Ecol, State Key Lab Marine Environm Sci, Xiamen 361005, Peoples R China
2.Nanjing Agr Univ, Coll Life Sci, Dept Microbiol, Key Lab Agr & Environm Microbiol,Minist Agr & Rur, Nanjing 210095, Peoples R China
3.NIH, Natl Lib Med, Bethesda, MD 20894 USA
4.Southern Univ Sci & Technol, Dept Ocean Sci & Engn, Shenzhen Key Lab Marine Archaea Geoom, Shenzhen 518055, Peoples R China
5.Shanghai Sheshan Natl Geophys Observ, Shanghai 201602, Peoples R China
6.Qingdao Univ, Coll Comp Sci & Technol, Qingdao 266101, Peoples R China
7.Univ Oklahoma, Inst Environm Genom, Sch Biol Sci, Norman, OK 73019 USA
8.Xiamen Univ, Coll Ocean & Earth Sci, State Key Lab Marine Environm Sci, Xiamen 361005, Peoples R China
9.Chinese Acad Sci, CAS Key Lab Urban Pollutant Convers, Inst Urban Environm, Xiamen 361021, Peoples R China
10.Shenzhen Univ, Inst Adv Study, Archaeal Biol Ctr, Shenzhen 518060, Peoples R China
11.Univ Washington, Dept Civil & Environm Engn, Seattle, WA 98195 USA
12.Univ Washington, Sch Oceanog, Seattle, WA 98195 USA
13.Univ Oklahoma, Sch Civil Engn & Environm Sci, Norman, OK 73019 USA
14.Lawrence Berkeley Natl Lab, Dept Earth & Environm Sci, Berkeley, CA 94720 USA
15.Univ Florida, Ft Lauderdale Res & Educ Ctr, Dept Microbiol & Cell Sci, Davie, FL 33314 USA

Zheng, Yue,Wang, Baozhan,Gao, Ping,et al. Novel order-level lineage of ammonia-oxidizing archaea widespread in marine and terrestrial environments[J]. ISME JOURNAL,2024,18(1).

Zheng, Yue.,Wang, Baozhan.,Gao, Ping.,Yang, Yiyan.,Xu, Bu.,...&Qin, Wei.(2024).Novel order-level lineage of ammonia-oxidizing archaea widespread in marine and terrestrial environments.ISME JOURNAL,18(1).

Zheng, Yue,et al."Novel order-level lineage of ammonia-oxidizing archaea widespread in marine and terrestrial environments".ISME JOURNAL 18.1(2024).