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:
-
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)
- 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}
}
Web of Science
Works referenced in this record:
The Plasma Membrane ATPase of Archaebacteria.: A Chimeric Energy Converter
journal, November 1992
- SchÁFer, GÜNter; Meyering-Vos, Martina
- Annals of the New York Academy of Sciences, Vol. 671, Issue 1 Ion-Motive AT
Lineages of Acidophilic Archaea Revealed by Community Genomic Analysis
journal, December 2006
- Baker, Brett J.; Tyson, Gene W.; Webb, Richard I.
- Science, Vol. 314, Issue 5807
Nitrogen cycling in forest soils across climate gradients in Eastern China
journal, January 2011
- Zhang, Jinbo; Zhu, Tongbin; Cai, Zucong
- Plant and Soil, Vol. 342, Issue 1-2
Cyanate as an energy source for nitrifiers
journal, July 2015
- Palatinszky, Marton; Herbold, Craig; Jehmlich, Nico
- Nature, Vol. 524, Issue 7563
Cultivation of a thermophilic ammonia oxidizing archaeon synthesizing crenarchaeol
journal, March 2008
- de la Torre, José R.; Walker, Christopher B.; Ingalls, Anitra E.
- Environmental Microbiology, Vol. 10, Issue 3
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
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
Urease gene-containing Archaea dominate autotrophic ammonia oxidation in two acid soils: Urea-linked archaeal ammonia oxidation in acid soil
journal, January 2013
- Lu, Lu; Jia, Zhongjun
- Environmental Microbiology, Vol. 15, Issue 6
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
Diversity and abundance of Crenarchaeota in terrestrial habitats studied by 16S RNA surveys and real time PCR
journal, September 2003
- Ochsenreiter, Torsten; Selezi, Drazenka; Quaiser, Achim
- Environmental Microbiology, Vol. 5, Issue 9
Soil microbial biomass and activity in Chinese tea gardens of varying stand age and productivity
journal, July 2007
- Han, Wenyan; Kemmitt, Sarah J.; Brookes, Philip C.
- Soil Biology and Biochemistry, Vol. 39, Issue 7
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
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
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
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
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
Production and characterization of cellulases and xylanases of Cellulosimicrobium cellulans grown in pretreated and extracted bagasse and minimal nutrient medium M9
journal, December 2010
- Song, Jian-Min; Wei, Dong-Zhi
- Biomass and Bioenergy, Vol. 34, Issue 12
Nitrosopumilus maritimus gen. nov., sp. nov., Nitrosopumilus cobalaminigenes sp. nov., Nitrosopumilus oxyclinae sp. nov., and Nitrosopumilus ureiphilus sp. nov., four marine ammonia-oxidizing archaea of the phylum Thaumarchaeota
journal, December 2017
- Qin, Wei; Heal, Katherine R.; Ramdasi, Rasika
- International Journal of Systematic and Evolutionary Microbiology, Vol. 67, Issue 12
Differential contributions of ammonia oxidizers and nitrite oxidizers to nitrification in four paddy soils
journal, October 2014
- Wang, Baozhan; Zhao, Jun; Guo, Zhiying
- The ISME Journal, Vol. 9, Issue 5
Archaea predominate among ammonia-oxidizing prokaryotes in soils
journal, August 2006
- Leininger, S.; Urich, T.; Schloter, M.
- Nature, Vol. 442, Issue 7104
The influence of soil pH on the diversity, abundance and transcriptional activity of ammonia oxidizing archaea and bacteria
journal, November 2008
- Nicol, Graeme W.; Leininger, Sven; Schleper, Christa
- Environmental Microbiology, Vol. 10, Issue 11
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
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
Changes in the community structure and activity of betaproteobacterial ammonia-oxidizing sediment bacteria along a freshwater-marine gradient
journal, April 2006
- Freitag, Thomas E.; Chang, Lisa; Prosser, James I.
- Environmental Microbiology, Vol. 8, Issue 4
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
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
Marsarchaeota are an aerobic archaeal lineage abundant in geothermal iron oxide microbial mats
journal, May 2018
- Jay, Zackary J.; Beam, Jacob P.; Dlakić, Mensur
- Nature Microbiology, Vol. 3, Issue 6
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
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
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
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
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
Factors influencing nitrification rates and the abundance and transcriptional activity of ammonia-oxidizing microorganisms in the dark northeast Pacific Ocean: Nitrification and AOA in the Dark Ocean
journal, December 2015
- Smith, Jason M.; Damashek, Julian; Chavez, Francisco P.
- Limnology and Oceanography, Vol. 61, Issue 2
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
Velvet: Algorithms for de novo short read assembly using de Bruijn graphs
journal, February 2008
- Zerbino, D. R.; Birney, E.
- Genome Research, Vol. 18, Issue 5
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
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
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
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
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
‘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
Candidatus Nitrosocaldus cavascurensis, an Ammonia Oxidizing, Extremely Thermophilic Archaeon with a Highly Mobile Genome
journal, January 2018
- Abby, Sophie S.; Melcher, Michael; Kerou, Melina
- Frontiers in Microbiology, Vol. 9
Crystal Structure of the Yeast Vacuolar ATPase Heterotrimeric EGChead Peripheral Stalk Complex
journal, November 2012
- Oot, Rebecca A.; Huang, Li-Shar; Berry, Edward A.
- Structure, Vol. 20, Issue 11
Accelerated Profile HMM Searches
journal, October 2011
- Eddy, Sean R.
- PLoS Computational Biology, Vol. 7, Issue 10
trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses
journal, June 2009
- Capella-Gutierrez, S.; Silla-Martinez, J. M.; Gabaldon, T.
- Bioinformatics, Vol. 25, Issue 15
Towards a Genome-Based Taxonomy for Prokaryotes
journal, September 2005
- Konstantinidis, K. T.; Tiedje, J. M.
- Journal of Bacteriology, Vol. 187, Issue 18
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
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
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
Analysis of intracellular pH in the yeast Saccharomyces cerevisiae under elevated hydrostatic pressure: a study in baro- (piezo-) physiology
journal, August 1998
- Abe, F.; Horikoshi, Koki
- Extremophiles, Vol. 2, Issue 3
Nitrification activity and putative ammonia-oxidizing archaea in acidic red soils
journal, December 2011
- Huang, Rong; Wu, Yucheng; Zhang, Jinbo
- Journal of Soils and Sediments, Vol. 12, Issue 3
Deep-sea piezosphere and piezophiles: geomicrobiology and biogeochemistry
journal, September 2010
- Fang, Jiasong; Zhang, Li; Bazylinski, Dennis A.
- Trends in Microbiology, Vol. 18, Issue 9
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
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
High hydrostatic pressure adaptive strategies in an obligate piezophile Pyrococcus yayanosii
journal, June 2016
- Michoud, Grégoire; Jebbar, Mohamed
- Scientific Reports, Vol. 6, Issue 1
Nitrification of archaeal ammonia oxidizers in acid soils is supported by hydrolysis of urea
journal, May 2012
- Lu, Lu; Han, Wenyan; Zhang, Jinbo
- The ISME Journal, Vol. 6, Issue 10
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
Methylotrophic methanogenesis discovered in the archaeal phylum Verstraetearchaeota
journal, October 2016
- Vanwonterghem, Inka; Evans, Paul N.; Parks, Donovan H.
- Nature Microbiology, Vol. 1, Issue 12
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
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
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
Cultivation and Genomic Analysis of “Candidatus Nitrosocaldus islandicus,” an Obligately Thermophilic, Ammonia-Oxidizing Thaumarchaeon from a Hot Spring Biofilm in Graendalur Valley, Iceland
journal, February 2018
- Daebeler, Anne; Herbold, Craig W.; Vierheilig, Julia
- Frontiers in Microbiology, Vol. 9
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
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
Phylogenomics of Cas4 family nucleases
journal, November 2017
- Hudaiberdiev, Sanjarbek; Shmakov, Sergey; Wolf, Yuri I.
- BMC Evolutionary Biology, Vol. 17, Issue 1
Nitrification in terrestrial hot springs of Iceland and Kamchatka: Nitrification in hot springs
journal, May 2008
- Reigstad, Laila J.; Richter, Andreas; Daims, Holger
- FEMS Microbiology Ecology, Vol. 64, Issue 2
Physiology and Diversity of Ammonia-Oxidizing Archaea
journal, October 2012
- Stahl, David A.; de la Torre, José R.
- Annual Review of Microbiology, Vol. 66, Issue 1
Pathways of Carbon Assimilation and Ammonia Oxidation Suggested by Environmental Genomic Analyses of Marine Crenarchaeota
journal, March 2006
- Hallam, Steven J.; Mincer, Tracy J.; Schleper, Christa
- PLoS Biology, Vol. 4, Issue 4, Article No. e95
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
14C2H2- and 14CO2-labeling studies of the de novo synthesis of polypeptides by Nitrosomonas europaea during recovery from acetylene and light inactivation of ammonia monooxygenase.
journal, January 1992
- Hyman, M. R.; Arp, D. J.
- Journal of Biological Chemistry, Vol. 267, Issue 3
Systematic discovery of pseudomonad genetic factors involved in sensitivity to tailocins
journal, March 2021
- Carim, Sean; Azadeh, Ashley L.; Kazakov, Alexey E.
- The ISME Journal, Vol. 15, Issue 8
Cloning of a Novel Pyrethroid-Hydrolyzing Carboxylesterase Gene from Sphingobium sp. Strain JZ-1 and Characterization of the Gene Product
journal, November 2009
- Wang, Bao-zhan; Guo, Peng; Hang, Bao-jian
- Applied and Environmental Microbiology, Vol. 75, Issue 22
Analysis of intracellular pH in the yeast Saccharomyces cerevisiae under elevated hydrostatic pressure: a study in baro- (piezo-) physiology
journal, August 1998
- Abe, F.; Horikoshi, Koki
- Extremophiles, Vol. 2, Issue 3
Horizontal transfer of ATPase genes — the tree of life becomes a net of life
journal, January 1993
- Hilario, Elena; Gogarten, Johann Peter
- Biosystems, Vol. 31, Issue 2-3
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
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
Soil microbial biomass and activity in Chinese tea gardens of varying stand age and productivity
journal, July 2007
- Han, Wenyan; Kemmitt, Sarah J.; Brookes, Philip C.
- Soil Biology and Biochemistry, Vol. 39, Issue 7
Crystal Structure of the Yeast Vacuolar ATPase Heterotrimeric EGChead Peripheral Stalk Complex
journal, November 2012
- Oot, Rebecca A.; Huang, Li-Shar; Berry, Edward A.
- Structure, Vol. 20, Issue 11
Deep-sea piezosphere and piezophiles: geomicrobiology and biogeochemistry
journal, September 2010
- Fang, Jiasong; Zhang, Li; Bazylinski, Dennis A.
- Trends in Microbiology, Vol. 18, Issue 9
The effect of high pressure upon proteins and other biomolecules
journal, February 1983
- Weber, Gregorio; Drickamer, Harry G.
- Quarterly Reviews of Biophysics, Vol. 16, Issue 1
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
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
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
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
Nitrification of archaeal ammonia oxidizers in acid soils is supported by hydrolysis of urea
journal, May 2012
- Lu, Lu; Han, Wenyan; Zhang, Jinbo
- The ISME Journal, Vol. 6, Issue 10
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
Differential contributions of ammonia oxidizers and nitrite oxidizers to nitrification in four paddy soils
journal, October 2014
- Wang, Baozhan; Zhao, Jun; Guo, Zhiying
- The ISME Journal, Vol. 9, Issue 5
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
Archaea predominate among ammonia-oxidizing prokaryotes in soils
journal, August 2006
- Leininger, S.; Urich, T.; Schloter, M.
- Nature, Vol. 442, Issue 7104
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
Cyanate as an energy source for nitrifiers
journal, July 2015
- Palatinszky, Marton; Herbold, Craig; Jehmlich, Nico
- Nature, Vol. 524, Issue 7563
Methylotrophic methanogenesis discovered in the archaeal phylum Verstraetearchaeota
journal, October 2016
- Vanwonterghem, Inka; Evans, Paul N.; Parks, Donovan H.
- Nature Microbiology, Vol. 1, Issue 12
‘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
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
Diversity and abundance of Crenarchaeota in terrestrial habitats studied by 16S RNA surveys and real time PCR
journal, September 2003
- Ochsenreiter, Torsten; Selezi, Drazenka; Quaiser, Achim
- Environmental Microbiology, Vol. 5, Issue 9
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
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
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
trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses
journal, June 2009
- Capella-Gutierrez, S.; Silla-Martinez, J. M.; Gabaldon, T.
- Bioinformatics, Vol. 25, Issue 15
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
Nitrosopumilus maritimus gen. nov., sp. nov., Nitrosopumilus cobalaminigenes sp. nov., Nitrosopumilus oxyclinae sp. nov., and Nitrosopumilus ureiphilus sp. nov., four marine ammonia-oxidizing archaea of the phylum Thaumarchaeota
journal, December 2017
- Qin, Wei; Heal, Katherine R.; Ramdasi, Rasika
- International Journal of Systematic and Evolutionary Microbiology, Vol. 67, Issue 12
The Archaeal Legacy of Eukaryotes: A Phylogenomic Perspective
journal, July 2014
- Guy, L.; Saw, J. H.; Ettema, T. J. G.
- Cold Spring Harbor Perspectives in Biology, Vol. 6, Issue 10
Velvet: Algorithms for de novo short read assembly using de Bruijn graphs
journal, February 2008
- Zerbino, D. R.; Birney, E.
- Genome Research, Vol. 18, Issue 5
Changes in the community structure and activity of betaproteobacterial ammonia-oxidizing sediment bacteria along a freshwater-marine gradient
journal, April 2006
- Freitag, Thomas E.; Chang, Lisa; Prosser, James I.
- Environmental Microbiology, Vol. 8, Issue 4
Cultivation of a thermophilic ammonia oxidizing archaeon synthesizing crenarchaeol
journal, March 2008
- de la Torre, José R.; Walker, Christopher B.; Ingalls, Anitra E.
- Environmental Microbiology, Vol. 10, Issue 3
The influence of soil pH on the diversity, abundance and transcriptional activity of ammonia oxidizing archaea and bacteria
journal, November 2008
- Nicol, Graeme W.; Leininger, Sven; Schleper, Christa
- Environmental Microbiology, Vol. 10, Issue 11
The Plasma Membrane ATPase of Archaebacteria.: A Chimeric Energy Converter
journal, November 1992
- SchÁFer, GÜNter; Meyering-Vos, Martina
- Annals of the New York Academy of Sciences, Vol. 671, Issue 1 Ion-Motive AT
Lineages of Acidophilic Archaea Revealed by Community Genomic Analysis
journal, December 2006
- Baker, Brett J.; Tyson, Gene W.; Webb, Richard I.
- Science, Vol. 314, Issue 5807
Updating Prokaryotic Taxonomy
journal, September 2005
- Rosselló-Mora, Ramon
- Journal of Bacteriology, Vol. 187, Issue 18
Physiology and Diversity of Ammonia-Oxidizing Archaea
journal, October 2012
- Stahl, David A.; de la Torre, José R.
- Annual Review of Microbiology, Vol. 66, Issue 1
Phylogenomics of Cas4 family nucleases
journal, November 2017
- Hudaiberdiev, Sanjarbek; Shmakov, Sergey; Wolf, Yuri I.
- BMC Evolutionary Biology, Vol. 17, Issue 1
Pathways of Carbon Assimilation and Ammonia Oxidation Suggested by Environmental Genomic Analyses of Marine Crenarchaeota
journal, March 2006
- Hallam, Steven J.; Mincer, Tracy J.; Schleper, Christa
- PLoS Biology, Vol. 4, Issue 4, Article No. e95
Accelerated Profile HMM Searches
journal, October 2011
- Eddy, Sean R.
- PLoS Computational Biology, Vol. 7, Issue 10
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
Works referencing / citing this record:
Simulating metagenomic stable isotope probing datasets with MetaSIPSim
journal, January 2020
- Barnett, Samuel E.; Buckley, Daniel H.
- BMC Bioinformatics, Vol. 21, Issue 1
Novel insights into the Thaumarchaeota in the deepest oceans: their metabolism and potential adaptation mechanisms
journal, June 2020
- Zhong, Haohui; Lehtovirta-Morley, Laura; Liu, Jiwen
- Microbiome, Vol. 8, Issue 1
Insight into the proteome of the hyperthermophilic Crenarchaeon Ignicoccus hospitalis: the major cytosolic and membrane proteins
journal, June 2008
- Burghardt, Tillmann; Saller, Manfred; Gürster, Sonja
- Archives of Microbiology, Vol. 190, Issue 3
Ignicoccus hospitalis and Nanoarchaeum equitans: ultrastructure, cell–cell interaction, and 3D reconstruction from serial sections of freeze-substituted cells and by electron cryotomography
journal, July 2008
- Junglas, Benjamin; Briegel, Ariane; Burghardt, Tillmann
- Archives of Microbiology, Vol. 190, Issue 3
‘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
Differential depth distribution of microbial function and putative symbionts through sediment-hosted aquifers in the deep terrestrial subsurface
journal, January 2018
- Probst, Alexander J.; Ladd, Bethany; Jarett, Jessica K.
- Nature Microbiology, Vol. 3, Issue 3
Archaeal phylogenomics provides evidence in support of a methanogenic origin of the Archaea and a thaumarchaeal origin for the eukaryotes
journal, September 2010
- Kelly, S.; Wickstead, B.; Gull, K.
- Proceedings of the Royal Society B: Biological Sciences, Vol. 278, Issue 1708
Nitrososphaera viennensis gen. nov., sp. nov., an aerobic and mesophilic, ammonia-oxidizing archaeon from soil and a member of the archaeal phylum Thaumarchaeota
journal, June 2014
- Stieglmeier, M.; Klingl, A.; Alves, R. J. E.
- INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 64, Issue Pt 8
Draft Genome Sequence of Halolamina pelagica CDK2 Isolated from Natural Salterns from Rann of Kutch, Gujarat, India
journal, February 2017
- Gaba, Sonam; Singh, Ram Nageena; Abrol, Shrutica
- Genome Announcements, Vol. 5, Issue 6
Activity and Metabolic Versatility of Complete Ammonia Oxidizers in Full-Scale Wastewater Treatment Systems
journal, April 2020
- Yang, Yuchun; Daims, Holger; Liu, Yang
- mBio, Vol. 11, Issue 2
Archaea in Natural and Impacted Brazilian Environments
journal, January 2016
- Rodrigues, Thiago; Belmok, Aline; Catão, Elisa
- Archaea, Vol. 2016
Birth of Archaeal Cells: Molecular Phylogenetic Analyses of G1P Dehydrogenase, G3P Dehydrogenases, and Glycerol Kinase Suggest Derived Features of Archaeal Membranes Having G1P Polar Lipids
journal, January 2016
- Yokobori, Shin-ichi; Nakajima, Yoshiki; Akanuma, Satoshi
- Archaea, Vol. 2016
Archaeal Community Changes Associated with Cultivation of Amazon Forest Soil with Oil Palm
journal, January 2016
- Tupinambá, Daiva Domenech; Cantão, Maurício Egídio; Costa, Ohana Yonara Assis
- Archaea, Vol. 2016
Genomic insights into an obligate epibiotic bacterial predator: Micavibrio aeruginosavorus ARL-13
journal, September 2011
- Wang, Zhang; Kadouri, Daniel E.; Wu, Martin
- BMC Genomics, Vol. 12, Issue 1
A pursuit of lineage-specific and niche-specific proteome features in the world of archaea
journal, January 2012
- Roy Chowdhury, Anindya; Dutta, Chitra
- BMC Genomics, Vol. 13, Issue 1
Analysis of Nanoarchaeum equitans genome and proteome composition: indications for hyperthermophilic and parasitic adaptation
journal, July 2006
- Das, Sabyasachi; Paul, Sandip; Bag, Sumit K.
- BMC Genomics, Vol. 7, Issue 1
Sequence analysis of an Archaeal virus isolated from a hypersaline lake in Inner Mongolia, China
journal, November 2007
- Pagaling, Eulyn; Haigh, Richard D.; Grant, William D.
- BMC Genomics, Vol. 8, Issue 1
SORGOdb: Superoxide Reductase Gene Ontology curated DataBase
journal, January 2011
- Lucchetti-Miganeh, Céline; Goudenège, David; Thybert, David
- BMC Microbiology, Vol. 11, Issue 1
The prokaryotic V4R domain is the likely ancestor of a key component of the eukaryotic vesicle transport system
journal, January 2008
- Podar, Mircea; Wall, Mark A.; Makarova, Kira S.
- Biology Direct, Vol. 3, Issue 1
Insights into archaeal evolution and symbiosis from the genomes of a nanoarchaeon and its inferred crenarchaeal host from Obsidian Pool, Yellowstone National Park
journal, April 2013
- Podar, Mircea; Makarova, Kira S.; Graham, David E.
- Biology Direct, Vol. 8, Issue 1
Minimization of extracellular space as a driving force in prokaryote association and the origin of eukaryotes
journal, January 2014
- Hooper, Scott L.; Burstein, Helaine J.
- Biology Direct, Vol. 9, Issue 1
Archaic chaos: intrinsically disordered proteins in Archaea
journal, May 2010
- Xue, Bin; Williams, Robert W.; Oldfield, Christopher J.
- BMC Systems Biology, Vol. 4, Issue S1
Breaking through a phylogenetic impasse: a pair of associated archaea might have played host in the endosymbiotic origin of eukaryotes
journal, January 2012
- Godde, James S.
- Cell & Bioscience, Vol. 2, Issue 1
Building on basic metagenomics with complementary technologies
journal, January 2007
- Warnecke, Falk; Hugenholtz, Philip
- Genome Biology, Vol. 8, Issue 12
Discovery of permuted and recently split transfer RNAs in Archaea
journal, April 2011
- Chan, Patricia P.; Cozen, Aaron E.; Lowe, Todd M.
- Genome Biology, Vol. 12, Issue 4
Happy together: genomic insights into the unique Nanoarchaeum/Ignicoccus association
journal, January 2009
- Forterre, Patrick; Gribaldo, Simonetta; Brochier-Armanet, Céline
- Journal of Biology, Vol. 8, Issue 1
Conservation of the C-type lectin fold for accommodating massive sequence variation in archaeal diversity-generating retroelements
journal, August 2016
- Handa, Sumit; Paul, Blair G.; Miller, Jeffery F.
- BMC Structural Biology, Vol. 16, Issue 1
Marine archaea and archaeal viruses under global change
journal, July 2017
- Danovaro, Roberto; Rastelli, Eugenio; Corinaldesi, Cinzia
- F1000Research, Vol. 6
Yellowstone Lake Nanoarchaeota
journal, January 2013
- Clingenpeel, Scott; Kan, Jinjun; Macur, Richard E.
- Frontiers in Microbiology, Vol. 4
Spatial variations of community structures and methane cycling across a transect of Lei-Gong-Hou mud volcanoes in eastern Taiwan
journal, March 2014
- Wang, Pei-Ling; Chiu, Yi-Ping; Cheng, Ting-Wen
- Frontiers in Microbiology, Vol. 5
S-layer and cytoplasmic membrane – exceptions from the typical archaeal cell wall with a focus on double membranes
journal, November 2014
- Klingl, Andreas
- Frontiers in Microbiology, Vol. 5
Inside Out: Archaeal Ectosymbionts Suggest a Second Model of Reduced-Genome Evolution
journal, March 2017
- Nicks, Trevor; Rahn-Lee, Lilah
- Frontiers in Microbiology, Vol. 8
A Complex Endomembrane System in the Archaeon Ignicoccus hospitalis Tapped by Nanoarchaeum equitans
journal, June 2017
- Heimerl, Thomas; Flechsler, Jennifer; Pickl, Carolin
- Frontiers in Microbiology, Vol. 8
Archaeal S-Layers: Overview and Current State of the Art
journal, December 2017
- Rodrigues-Oliveira, Thiago; Belmok, Aline; Vasconcellos, Deborah
- Frontiers in Microbiology, Vol. 8
Nano-Sized and Filterable Bacteria and Archaea: Biodiversity and Function
journal, August 2018
- Ghuneim, Lydia-Ann J.; Jones, David L.; Golyshin, Peter N.
- Frontiers in Microbiology, Vol. 9
A Multi-Functional Tubulovesicular Network as the Ancestral Eukaryotic Endomembrane System
journal, March 2015
- González-Sánchez, Juan; Costa, Ricardo; Devos, Damien
- Biology, Vol. 4, Issue 2
Diversity of “Ca. Micrarchaeota” in Two Distinct Types of Acidic Environments and Their Associations with Thermoplasmatales
journal, June 2019
- Golyshina, Olga V.; Bargiela, Rafael; Toshchakov, Stepan V.
- Genes, Vol. 10, Issue 6
Anaerobic Thermophiles
journal, February 2014
- Canganella, Francesco; Wiegel, Juergen
- Life, Vol. 4, Issue 1
Biota and Biomolecules in Extreme Environments on Earth: Implications for Life Detection on Mars
journal, October 2014
- Aerts, Joost; Röling, Wilfred; Elsaesser, Andreas
- Life, Vol. 4, Issue 4
Archaeal Clusters of Orthologous Genes (arCOGs): An Update and Application for Analysis of Shared Features between Thermococcales, Methanococcales, and Methanobacteriales
journal, March 2015
- Makarova, Kira; Wolf, Yuri; Koonin, Eugene
- Life, Vol. 5, Issue 1
Small regulatory RNAs in Archaea
journal, March 2014
- Babski, Julia; Maier, Lisa-Katharina; Heyer, Ruth
- RNA Biology, Vol. 11, Issue 5
Grappling archaea: ultrastructural analyses of an uncultivated, cold-loving archaeon and its biofilm
text, January 2014
- Moissl-Eichinger, Christine; Perras, Alexandra K.; Wanner, Gerhard
- Universität Regensburg