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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 Lab. (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. 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., & 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 = {2019},
month = {8}
}

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Works referenced in this record:

The Plasma Membrane ATPase of Archaebacteria.: A Chimeric Energy Converter
journal, November 1992


Lineages of Acidophilic Archaea Revealed by Community Genomic Analysis
journal, December 2006


Nitrogen cycling in forest soils across climate gradients in Eastern China
journal, January 2011


Cyanate as an energy source for nitrifiers
journal, July 2015

  • Palatinszky, Marton; Herbold, Craig; Jehmlich, Nico
  • Nature, Vol. 524, Issue 7563
  • DOI: 10.1038/nature14856

Cultivation of a thermophilic ammonia oxidizing archaeon synthesizing crenarchaeol
journal, March 2008


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
  • DOI: 10.1073/pnas.0506625102

A moderately thermophilic ammonia-oxidizing crenarchaeote from a hot spring
journal, February 2008

  • Hatzenpichler, R.; Lebedeva, E. V.; Spieck, E.
  • Proceedings of the National Academy of Sciences, Vol. 105, Issue 6
  • DOI: 10.1073/pnas.0708857105

Pressure dependence of weak acid ionization in aqueous buffers
journal, October 1973

  • Neuman, Robert C.; Kauzmann, Walter; Zipp, Adam
  • The Journal of Physical Chemistry, Vol. 77, Issue 22
  • DOI: 10.1021/j100640a025

Diversity and abundance of Crenarchaeota in terrestrial habitats studied by 16S RNA surveys and real time PCR
journal, September 2003


Soil microbial biomass and activity in Chinese tea gardens of varying stand age and productivity
journal, July 2007


Coupling of diversification and pH adaptation during the evolution of terrestrial Thaumarchaeota
journal, July 2015

  • Gubry-Rangin, Cécile; Kratsch, Christina; Williams, Tom A.
  • Proceedings of the National Academy of Sciences, Vol. 112, Issue 30
  • DOI: 10.1073/pnas.1419329112

Nitrososphaera viennensis, an ammonia oxidizing archaeon from soil
journal, April 2011

  • Tourna, M.; Stieglmeier, M.; Spang, A.
  • Proceedings of the National Academy of Sciences, Vol. 108, Issue 20
  • DOI: 10.1073/pnas.1013488108

Evolution of the vacuolar H+-ATPase: implications for the origin of eukaryotes.
journal, September 1989

  • Gogarten, J. P.; Kibak, H.; Dittrich, P.
  • Proceedings of the National Academy of Sciences, Vol. 86, Issue 17
  • DOI: 10.1073/pnas.86.17.6661

ATP synthases from archaea: The beauty of a molecular motor
journal, June 2014

  • Grüber, Gerhard; Manimekalai, Malathy Sony Subramanian; Mayer, Florian
  • Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1837, Issue 6
  • DOI: 10.1016/j.bbabio.2014.03.004

Crystal structures of aspartate carbamoyltransferase ligated with phosphonoacetamide, malonate, and CTP or ATP at 2.8-.ANG. resolution and neutral pH
journal, August 1990

  • Gouaux, J. Eric; Stevens, Raymond C.; Lipscomb, William N.
  • Biochemistry, Vol. 29, Issue 33
  • DOI: 10.1021/bi00485a020

Differential contributions of ammonia oxidizers and nitrite oxidizers to nitrification in four paddy soils
journal, October 2014


Archaea predominate among ammonia-oxidizing prokaryotes in soils
journal, August 2006


The influence of soil pH on the diversity, abundance and transcriptional activity of ammonia oxidizing archaea and bacteria
journal, November 2008


Hadal biosphere: Insight into the microbial ecosystem in the deepest ocean on Earth
journal, February 2015

  • Nunoura, Takuro; Takaki, Yoshihiro; Hirai, Miho
  • Proceedings of the National Academy of Sciences, Vol. 112, Issue 11
  • DOI: 10.1073/pnas.1421816112

Bioenergetics of archaea: Ancient energy conserving mechanisms developed in the early history of life
journal, May 2006

  • Lewalter, Kim; Müller, Volker
  • Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1757, Issue 5-6
  • DOI: 10.1016/j.bbabio.2006.04.027

Changes in the community structure and activity of betaproteobacterial ammonia-oxidizing sediment bacteria along a freshwater-marine gradient
journal, April 2006


Cultivation of an obligate acidophilic ammonia oxidizer from a nitrifying acid soil
journal, September 2011

  • Lehtovirta-Morley, L. E.; Stoecker, K.; Vilcinskas, A.
  • Proceedings of the National Academy of Sciences, Vol. 108, Issue 38
  • DOI: 10.1073/pnas.1107196108

Structural Basis for a Unique ATP Synthase Core Complex from Nanoarcheaum equitans
journal, September 2015

  • Mohanty, Soumya; Jobichen, Chacko; Chichili, Vishnu Priyanka Reddy
  • Journal of Biological Chemistry, Vol. 290, Issue 45
  • DOI: 10.1074/jbc.M115.677492

Marsarchaeota are an aerobic archaeal lineage abundant in geothermal iron oxide microbial mats
journal, May 2018


CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes
journal, May 2015

  • Parks, Donovan H.; Imelfort, Michael; Skennerton, Connor T.
  • Genome Research, Vol. 25, Issue 7
  • DOI: 10.1101/gr.186072.114

Prokaryotic responses to hydrostatic pressure in the ocean - a review: Prokaryotic responses to pressure in the ocean
journal, February 2013

  • Tamburini, Christian; Boutrif, Mehdi; Garel, Marc
  • Environmental Microbiology, Vol. 15, Issue 5
  • DOI: 10.1111/1462-2920.12084

Examining the global distribution of dominant archaeal populations in soil
journal, November 2010

  • Bates, Scott T.; Berg-Lyons, Donna; Caporaso, J. Gregory
  • The ISME Journal, Vol. 5, Issue 5
  • DOI: 10.1038/ismej.2010.171

Niche specialization of novel Thaumarchaeota to oxic and hypoxic acidic geothermal springs of Yellowstone National Park
journal, November 2013

  • Beam, Jacob P.; Jay, Zackary J.; Kozubal, Mark A.
  • The ISME Journal, Vol. 8, Issue 4
  • DOI: 10.1038/ismej.2013.193

A new phylum of Archaea represented by a nanosized hyperthermophilic symbiont
journal, May 2002

  • Huber, Harald; Hohn, Michael J.; Rachel, Reinhard
  • Nature, Vol. 417, Issue 6884
  • DOI: 10.1038/417063a

MAFFT Multiple Sequence Alignment Software Version 7: Improvements in Performance and Usability
journal, January 2013

  • Katoh, K.; Standley, D. M.
  • Molecular Biology and Evolution, Vol. 30, Issue 4
  • DOI: 10.1093/molbev/mst010

Velvet: Algorithms for de novo short read assembly using de Bruijn graphs
journal, February 2008


IQ-TREE: A Fast and Effective Stochastic Algorithm for Estimating Maximum-Likelihood Phylogenies
journal, November 2014

  • Nguyen, Lam-Tung; Schmidt, Heiko A.; von Haeseler, Arndt
  • Molecular Biology and Evolution, Vol. 32, Issue 1
  • DOI: 10.1093/molbev/msu300

Ammonia-oxidising archaea living at low pH: Insights from comparative genomics: Comparative genomics of ammonia-oxidising archaea
journal, December 2017

  • Herbold, Craig W.; Lehtovirta-Morley, Laura E.; Jung, Man-Young
  • Environmental Microbiology, Vol. 19, Issue 12
  • DOI: 10.1111/1462-2920.13971

Global Biodiversity of Aquatic Ammonia-Oxidizing Archaea is Partitioned by Habitat
journal, January 2012

  • Biller, Steven J.; Mosier, Annika C.; Wells, George F.
  • Frontiers in Microbiology, Vol. 3
  • DOI: 10.3389/fmicb.2012.00252

Horizontal transfer of ATPase genes — the tree of life becomes a net of life
journal, January 1993


Genomics insights into ecotype formation of ammonia-oxidizing archaea in the deep ocean: Genomics of MGI AOA lineages
journal, January 2019

  • Wang, Yong; Huang, Jiao-Mei; Cui, Guo-Jie
  • Environmental Microbiology, Vol. 21, Issue 2
  • DOI: 10.1111/1462-2920.14518

Inventing the dynamo machine: the evolution of the F-type and V-type ATPases
journal, November 2007

  • Mulkidjanian, Armen Y.; Makarova, Kira S.; Galperin, Michael Y.
  • Nature Reviews Microbiology, Vol. 5, Issue 11
  • DOI: 10.1038/nrmicro1767

‘ARMAN’ archaea depend on association with euryarchaeal host in culture and in situ
journal, July 2017

  • Golyshina, Olga V.; Toshchakov, Stepan V.; Makarova, Kira S.
  • Nature Communications, Vol. 8, Issue 1
  • DOI: 10.1038/s41467-017-00104-7

Candidatus Nitrosocaldus cavascurensis, an Ammonia Oxidizing, Extremely Thermophilic Archaeon with a Highly Mobile Genome
journal, January 2018


Crystal Structure of the Yeast Vacuolar ATPase Heterotrimeric EGChead Peripheral Stalk Complex
journal, November 2012


Accelerated Profile HMM Searches
journal, October 2011


trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses
journal, June 2009


Towards a Genome-Based Taxonomy for Prokaryotes
journal, September 2005


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
  • DOI: 10.1038/s41564-018-0316-2

Geographic Distribution of Archaeal Ammonia Oxidizing Ecotypes in the Atlantic Ocean
journal, February 2016

  • Sintes, Eva; De Corte, Daniele; Haberleitner, Elisabeth
  • Frontiers in Microbiology, Vol. 7
  • DOI: 10.3389/fmicb.2016.00077

Single Cells within the Puerto Rico Trench Suggest Hadal Adaptation of Microbial Lineages
journal, September 2015

  • León-Zayas, Rosa; Novotny, Mark; Podell, Sheila
  • Applied and Environmental Microbiology, Vol. 81, Issue 24
  • DOI: 10.1128/AEM.01659-15

Nitrification activity and putative ammonia-oxidizing archaea in acidic red soils
journal, December 2011


Deep-sea piezosphere and piezophiles: geomicrobiology and biogeochemistry
journal, September 2010


Genomic and proteomic characterization of “ Candidatus Nitrosopelagicus brevis”: An ammonia-oxidizing archaeon from the open ocean
journal, January 2015

  • Santoro, Alyson E.; Dupont, Christopher L.; Richter, R. Alex
  • Proceedings of the National Academy of Sciences, Vol. 112, Issue 4
  • DOI: 10.1073/pnas.1416223112

Ultrafast Approximation for Phylogenetic Bootstrap
journal, February 2013

  • Minh, B. Q.; Nguyen, M. A. T.; von Haeseler, A.
  • Molecular Biology and Evolution, Vol. 30, Issue 5
  • DOI: 10.1093/molbev/mst024

High hydrostatic pressure adaptive strategies in an obligate piezophile Pyrococcus yayanosii
journal, June 2016

  • Michoud, Grégoire; Jebbar, Mohamed
  • Scientific Reports, Vol. 6, Issue 1
  • DOI: 10.1038/srep27289

Nitrification of archaeal ammonia oxidizers in acid soils is supported by hydrolysis of urea
journal, May 2012


Cloning of a Novel Pyrethroid-Hydrolyzing Carboxylesterase Gene from Sphingobium sp. Strain JZ-1 and Characterization of the Gene Product
journal, July 2009

  • Wang, B. -z.; Guo, P.; Hang, B. -j.
  • Applied and Environmental Microbiology, Vol. 75, Issue 17
  • DOI: 10.1128/AEM.01298-09

Methylotrophic methanogenesis discovered in the archaeal phylum Verstraetearchaeota
journal, October 2016


Archaeal dominance in the mesopelagic zone of the Pacific Ocean
journal, January 2001

  • Karner, Markus B.; DeLong, Edward F.; Karl, David M.
  • Nature, Vol. 409, Issue 6819
  • DOI: 10.1038/35054051

The effect of high pressure upon proteins and other biomolecules
journal, February 1983


Isolation of an autotrophic ammonia-oxidizing marine archaeon
journal, September 2005

  • Könneke, Martin; Bernhard, Anne E.; de la Torre, José R.
  • Nature, Vol. 437, Issue 7058
  • DOI: 10.1038/nature03911

A hydrophobic ammonia-oxidizing archaeon of the Nitrosocosmicus clade isolated from coal tar-contaminated sediment : Ecophysiological properties of a hydrophobic AOA
journal, October 2016

  • Jung, Man-Young; Kim, Jong-Geol; Sinninghe Damsté, Jaap S.
  • Environmental Microbiology Reports, Vol. 8, Issue 6
  • DOI: 10.1111/1758-2229.12477

Complex archaea that bridge the gap between prokaryotes and eukaryotes
journal, May 2015

  • Spang, Anja; Saw, Jimmy H.; Jørgensen, Steffen L.
  • Nature, Vol. 521, Issue 7551
  • DOI: 10.1038/nature14447

A Sulfurtransferase Is Required in the Transfer of Cysteine Sulfur in the in Vitro Synthesis of Molybdopterin from Precursor Z in Escherichia coli
journal, April 2001

  • Leimkühler, Silke; Rajagopalan, K. V.
  • Journal of Biological Chemistry, Vol. 276, Issue 25
  • DOI: 10.1074/jbc.M102072200

Phylogenomics of Cas4 family nucleases
journal, November 2017

  • Hudaiberdiev, Sanjarbek; Shmakov, Sergey; Wolf, Yuri I.
  • BMC Evolutionary Biology, Vol. 17, Issue 1
  • DOI: 10.1186/s12862-017-1081-1

Nitrification in terrestrial hot springs of Iceland and Kamchatka: Nitrification in hot springs
journal, May 2008


Physiology and Diversity of Ammonia-Oxidizing Archaea
journal, October 2012


Pathways of Carbon Assimilation and Ammonia Oxidation Suggested by Environmental Genomic Analyses of Marine Crenarchaeota
journal, March 2006


Enigmatic, ultrasmall, uncultivated Archaea
journal, April 2010

  • Baker, B. J.; Comolli, L. R.; Dick, G. J.
  • Proceedings of the National Academy of Sciences, Vol. 107, Issue 19
  • DOI: 10.1073/pnas.0914470107

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