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

Abstract

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.

Authors:
 [1];  [2];  [3];  [4]; ORCiD logo [5];  [5]; ORCiD logo [6];  [7];  [8];  [4];  [9];  [9];  [7];  [3];  [10];  [10];  [11];  [5];  [12];  [13] more »;  [14];  [2]; ORCiD logo [15];  [2];  [4] « less
  1. Chinese Academy of Sciences (CAS), Nanjing (China); Univ. of Vienna (Austria)
  2. Univ. of Washington, Seattle, WA (United States)
  3. Shanghai Majorbio Bio-pharm Biotechnology Co., Ltd, Shanghai (China)
  4. Chinese Academy of Sciences (CAS), Nanjing (China)
  5. Univ. of Vienna (Austria)
  6. Univ. of California, San Diego, La Jolla, CA (United States); USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
  7. Shenzhen Univ. (China)
  8. Chinese Academy of Sciences (CAS), Xiamen (China)
  9. Nanjing Agricultural Univ. (China)
  10. Pacific Biosciences, Menlo Park, CA (United States)
  11. Univ. of Florida, Gainesville, FL (United States)
  12. Chungbuk National Univ., Cheongju (South Korea)
  13. Univ. of California, San Diego, La Jolla, CA (United States)
  14. Chinese Academy of Sciences (CAS), Beijing (China)
  15. Univ. of Vienna (Austria); Aalborg Univ. (Denmark)
Publication Date:
Research Org.:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC); National Science Foundation (NSF); Genomic Science and Technology for Energy and Environment; European Research Council (ERC)
OSTI Identifier:
1591838
Grant/Contract Number:  
AC02-05CH11231; MCB-0604448; SC0006869; 294343
Resource Type:
Accepted Manuscript
Journal Name:
The ISME Journal
Additional Journal Information:
Journal Volume: 13; Journal Issue: 12; Journal ID: ISSN 1751-7362
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; metagenomics; microbial ecology

Citation Formats

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., and Jia, Zhongjun. Expansion of Thaumarchaeota habitat range is correlated with horizontal transfer of ATPase operons. United States: N. p., 2019. Web. doi:10.1038/s41396-019-0493-x.
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. Expansion of Thaumarchaeota habitat range is correlated with horizontal transfer of ATPase operons. United States. https://doi.org/10.1038/s41396-019-0493-x
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., and Jia, Zhongjun. Wed . "Expansion of Thaumarchaeota habitat range is correlated with horizontal transfer of ATPase operons". United States. https://doi.org/10.1038/s41396-019-0493-x. https://www.osti.gov/servlets/purl/1591838.
@article{osti_1591838,
title = {Expansion of Thaumarchaeota habitat range is correlated with horizontal transfer of ATPase operons},
author = {Wang, Baozhan and Qin, Wei and Ren, Yi and Zhou, Xue and Jung, Man-Young and Han, Ping and Eloe-Fadrosh, Emiley A. and Li, Meng and Zheng, Yue and Lu, Lu and Yan, Xin and Ji, Junbin and Liu, Yang and Liu, Linmeng and Heiner, Cheryl and Hall, Richard and Martens-Habbena, Willm and Herbold, Craig W. and Rhee, Sung-keun and Bartlett, Douglas H. and Huang, Li and Ingalls, Anitra E. and Wagner, Michael and Stahl, David A. and Jia, Zhongjun},
abstractNote = {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.},
doi = {10.1038/s41396-019-0493-x},
journal = {The ISME Journal},
number = 12,
volume = 13,
place = {United States},
year = {Wed Aug 28 00:00:00 EDT 2019},
month = {Wed Aug 28 00:00:00 EDT 2019}
}

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Archaea predominate among ammonia-oxidizing prokaryotes in soils
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Complex archaea that bridge the gap between prokaryotes and eukaryotes
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Cyanate as an energy source for nitrifiers
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  • Nature, Vol. 524, Issue 7563
  • DOI: 10.1038/nature14856

Methylotrophic methanogenesis discovered in the archaeal phylum Verstraetearchaeota
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‘ARMAN’ archaea depend on association with euryarchaeal host in culture and in situ
journal, July 2017

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  • Nature Communications, Vol. 8, Issue 1
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Cyanate and urea are substrates for nitrification by Thaumarchaeota in the marine environment
journal, December 2018

  • Kitzinger, Katharina; Padilla, Cory C.; Marchant, Hannah K.
  • Nature Microbiology, Vol. 4, Issue 2
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Diversity and abundance of Crenarchaeota in terrestrial habitats studied by 16S RNA surveys and real time PCR
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Ubiquity and diversity of ammonia-oxidizing archaea in water columns and sediments of the ocean
journal, September 2005

  • Francis, C. A.; Roberts, K. J.; Beman, J. M.
  • Proceedings of the National Academy of Sciences, Vol. 102, Issue 41, p. 14683-14688
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Nitrososphaera viennensis, an ammonia oxidizing archaeon from soil
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Cultivation of an obligate acidophilic ammonia oxidizer from a nitrifying acid soil
journal, September 2011

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  • Proceedings of the National Academy of Sciences, Vol. 108, Issue 38
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