Expansion of Thaumarchaeota habitat range is correlated with horizontal transfer of ATPase operons

Wang, Baozhan; Qin, Wei; Ren, Yi; Zhou, Xue; Jung, Man-Young; Han, Ping; Eloe-Fadrosh, Emiley A.; Li, Meng; Zheng, Yue; Lu, Lu; Yan, Xin; Ji, Junbin; Liu, Yang; Liu, Linmeng; Heiner, Cheryl; Hall, Richard; Martens-Habbena, Willm; Herbold, Craig W.; Rhee, Sung-keun; Bartlett, Douglas H.; Huang, Li; Ingalls, Anitra E.; Wagner, Michael; Stahl, David A.; Jia, Zhongjun

doi:10.1038/s41396-019-0493-x

Title: Expansion of Thaumarchaeota habitat range is correlated with horizontal transfer of ATPase operons

Journal Article · 28 August 2019 · The ISME Journal

DOI: https://doi.org/10.1038/s41396-019-0493-x · OSTI ID:1591838

Wang, Baozhan ^[1]; Qin, Wei ^[2]; Ren, Yi ^[3]; Zhou, Xue ^[4];

^[5]; Han, Ping ^[5];

^[6]; Li, Meng ^[7]; Zheng, Yue ^[8]; Lu, Lu ^[4]; Yan, Xin ^[9]; Ji, Junbin ^[9]; Liu, Yang ^[7]; Liu, Linmeng ^[3]; Heiner, Cheryl ^[10]; Hall, Richard ^[10]; Martens-Habbena, Willm ^[11]; Herbold, Craig W. ^[5]; Rhee, Sung-keun ^[12]; Bartlett, Douglas H. ^[13] more »

Chinese Academy of Sciences (CAS), Nanjing (China); Univ. of Vienna (Austria)
Univ. of Washington, Seattle, WA (United States)
Shanghai Majorbio Bio-pharm Biotechnology Co., Ltd, Shanghai (China)
Chinese Academy of Sciences (CAS), Nanjing (China)
Univ. of Vienna (Austria)
Univ. of California, San Diego, La Jolla, CA (United States); USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
Shenzhen Univ. (China)
Chinese Academy of Sciences (CAS), Xiamen (China)
Nanjing Agricultural Univ. (China)
Pacific Biosciences, Menlo Park, CA (United States)
Univ. of Florida, Gainesville, FL (United States)
Chungbuk National Univ., Cheongju (South Korea)
Univ. of California, San Diego, La Jolla, CA (United States)
Chinese Academy of Sciences (CAS), Beijing (China)
Univ. of Vienna (Austria); Aalborg Univ. (Denmark)

Thaumarchaeota are responsible for a significant fraction of ammonia oxidation in the oceans and in soils that range from alkaline to acidic. However, the adaptive mechanisms underpinning their habitat expansion remain poorly understood. Here we show that expansion into acidic soils and the high pressures of the hadopelagic zone of the oceans is tightly linked to the acquisition of a variant of the energy-yielding ATPases via horizontal transfer. Whereas the ATPase genealogy of neutrophilic Thaumarchaeota is congruent with their organismal genealogy inferred from concatenated conserved proteins, a common clade of V-type ATPases unites phylogenetically distinct clades of acidophilic/acid-tolerant and piezophilic/piezotolerant species. A presumptive function of pumping cytoplasmic protons at low pH is consistent with the experimentally observed increased expression of the V-ATPase in an acid-tolerant thaumarchaeote at low pH. Consistently, heterologous expression of the thaumarchaeotal V-ATPase significantly increased the growth rate of E. coli at low pH. Its adaptive significance to growth in ocean trenches may relate to pressure-related changes in membrane structure in which this complex molecular machine must function. Together, our findings reveal that the habitat expansion of Thaumarchaeota is tightly correlated with extensive horizontal transfer of atp operons.

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Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC); National Science Foundation (NSF); Genomic Science and Technology for Energy and Environment; European Research Council (ERC)

Grant/Contract Number:: AC02-05CH11231; MCB-0604448; SC0006869; 294343

OSTI ID:: 1591838

Journal Information:: The ISME Journal, Vol. 13, Issue 12; ISSN 1751-7362

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 41 works

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