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Title: Ammonia‐oxidising archaea living at low pH: Insights from comparative genomics

Abstract

Summary Obligate acidophilic members of the thaumarchaeotal genus Candidatus Nitrosotalea play an important role in nitrification in acidic soils, but their evolutionary and physiological adaptations to acidic environments are still poorly understood, with only a single member of this genus ( Ca . N. devanaterra) having its genome sequenced. In this study, we sequenced the genomes of two additional cultured Ca . Nitrosotalea strains, extracted an almost complete Ca . Nitrosotalea metagenome‐assembled genome from an acidic fen, and performed comparative genomics of the four Ca . Nitrosotalea genomes with 19 other archaeal ammonia oxidiser genomes. Average nucleotide and amino acid identities revealed that the four Ca . Nitrosotalea strains represent separate species within the genus. The four Ca . Nitrosotalea genomes contained a core set of 103 orthologous gene families absent from all other ammonia‐oxidizing archaea and, for most of these gene families, expression could be demonstrated in laboratory culture or the environment via proteomic or metatranscriptomic analyses respectively. Phylogenetic analyses indicated that four of these core gene families were acquired by the Ca . Nitrosotalea common ancestor via horizontal gene transfer from acidophilic representatives of Euryarchaeota. We hypothesize that gene exchange with these acidophiles contributed to the competitive successmore » of the Ca . Nitrosotalea lineage in acidic environments.« less

Authors:
ORCiD logo [1]; ORCiD logo [2];  [3];  [4]; ORCiD logo [1];  [1]; ORCiD logo [1];  [5];  [6];  [3];  [7];  [8]; ORCiD logo [1]; ORCiD logo [7]
  1. Division of Microbial Ecology, Department of Microbiology and Ecosystem Science Research Network Chemistry meets Microbiology, University of Vienna Vienna Austria
  2. School of Biological Sciences University of East Anglia, Norwich Research Park Norwich NR4 7TJ UK, School of Biological Sciences University of Aberdeen, Cruickshank Building, St Machar Drive Aberdeen AB24 3UU UK
  3. Department of Microbiology Chungbuk National University, 1 Chungdae‐ro, Seowon‐Gu Cheongju 362‐763 South Korea
  4. Department of Molecular Systems Biology Helmholtz‐Centre for Environmental Research‐UFZ Leipzig 04318 Germany
  5. Department of Microorganisms Leibniz Institute DSMZ ‐ German Collection of Microorganisms and Cell Cultures Inhoffenstr. 7B Braunschweig 38124 Germany
  6. Department of Botany and Plant Pathology Oregon State University, 2082 Cordley Hall Corvallis OR 97331‐2902 USA
  7. School of Biological Sciences University of Aberdeen, Cruickshank Building, St Machar Drive Aberdeen AB24 3UU UK
  8. Laboratoire Ampère, École Centrale de Lyon, L'Université de Lyon, 36 avenue Guy de Collongue 69134 Ecully CEDEX France
Publication Date:
Research Org.:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE
OSTI Identifier:
1411259
Alternate Identifier(s):
OSTI ID: 1411477; OSTI ID: 1625851
Grant/Contract Number:  
AC02-05CH11231
Resource Type:
Published Article
Journal Name:
Environmental Microbiology
Additional Journal Information:
Journal Name: Environmental Microbiology Journal Volume: 19 Journal Issue: 12; Journal ID: ISSN 1462-2912
Publisher:
Wiley-Blackwell
Country of Publication:
United Kingdom
Language:
English
Subject:
Microbiology

Citation Formats

Herbold, Craig W., Lehtovirta‐Morley, Laura E., Jung, Man‐Young, Jehmlich, Nico, Hausmann, Bela, Han, Ping, Loy, Alexander, Pester, Michael, Sayavedra‐Soto, Luis A., Rhee, Sung‐Keun, Prosser, James I., Nicol, Graeme W., Wagner, Michael, and Gubry‐Rangin, Cécile. Ammonia‐oxidising archaea living at low pH: Insights from comparative genomics. United Kingdom: N. p., 2017. Web. doi:10.1111/1462-2920.13971.
Herbold, Craig W., Lehtovirta‐Morley, Laura E., Jung, Man‐Young, Jehmlich, Nico, Hausmann, Bela, Han, Ping, Loy, Alexander, Pester, Michael, Sayavedra‐Soto, Luis A., Rhee, Sung‐Keun, Prosser, James I., Nicol, Graeme W., Wagner, Michael, & Gubry‐Rangin, Cécile. Ammonia‐oxidising archaea living at low pH: Insights from comparative genomics. United Kingdom. https://doi.org/10.1111/1462-2920.13971
Herbold, Craig W., Lehtovirta‐Morley, Laura E., Jung, Man‐Young, Jehmlich, Nico, Hausmann, Bela, Han, Ping, Loy, Alexander, Pester, Michael, Sayavedra‐Soto, Luis A., Rhee, Sung‐Keun, Prosser, James I., Nicol, Graeme W., Wagner, Michael, and Gubry‐Rangin, Cécile. Mon . "Ammonia‐oxidising archaea living at low pH: Insights from comparative genomics". United Kingdom. https://doi.org/10.1111/1462-2920.13971.
@article{osti_1411259,
title = {Ammonia‐oxidising archaea living at low pH: Insights from comparative genomics},
author = {Herbold, Craig W. and Lehtovirta‐Morley, Laura E. and Jung, Man‐Young and Jehmlich, Nico and Hausmann, Bela and Han, Ping and Loy, Alexander and Pester, Michael and Sayavedra‐Soto, Luis A. and Rhee, Sung‐Keun and Prosser, James I. and Nicol, Graeme W. and Wagner, Michael and Gubry‐Rangin, Cécile},
abstractNote = {Summary Obligate acidophilic members of the thaumarchaeotal genus Candidatus Nitrosotalea play an important role in nitrification in acidic soils, but their evolutionary and physiological adaptations to acidic environments are still poorly understood, with only a single member of this genus ( Ca . N. devanaterra) having its genome sequenced. In this study, we sequenced the genomes of two additional cultured Ca . Nitrosotalea strains, extracted an almost complete Ca . Nitrosotalea metagenome‐assembled genome from an acidic fen, and performed comparative genomics of the four Ca . Nitrosotalea genomes with 19 other archaeal ammonia oxidiser genomes. Average nucleotide and amino acid identities revealed that the four Ca . Nitrosotalea strains represent separate species within the genus. The four Ca . Nitrosotalea genomes contained a core set of 103 orthologous gene families absent from all other ammonia‐oxidizing archaea and, for most of these gene families, expression could be demonstrated in laboratory culture or the environment via proteomic or metatranscriptomic analyses respectively. Phylogenetic analyses indicated that four of these core gene families were acquired by the Ca . Nitrosotalea common ancestor via horizontal gene transfer from acidophilic representatives of Euryarchaeota. We hypothesize that gene exchange with these acidophiles contributed to the competitive success of the Ca . Nitrosotalea lineage in acidic environments.},
doi = {10.1111/1462-2920.13971},
journal = {Environmental Microbiology},
number = 12,
volume = 19,
place = {United Kingdom},
year = {Mon Dec 04 00:00:00 EST 2017},
month = {Mon Dec 04 00:00:00 EST 2017}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record
https://doi.org/10.1111/1462-2920.13971

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Cited by: 63 works
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Figures / Tables:

Fig. 1 Fig. 1: Heat maps showing pairwise ANI and AAI values inferred from the four Ca. Nitrosotalea genomes (bold) and other available Thaumarchaeota genomes. Dendrograms were calculated by hierarchical clustering (hclust, method = complete linkage) in R with distances calculated as (100% – % identity, that is, 100% ANI = 0more » distance). For ANI and AAI, values above 70% and 60%, respectively, are indicated on the heat map.« less

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Works referenced in this record:

REAPR: a universal tool for genome assembly evaluation
journal, January 2013


An acid-tolerant ammonia-oxidizing γ-proteobacterium from soil
journal, January 2017

  • Hayatsu, Masahito; Tago, Kanako; Uchiyama, Ikuo
  • The ISME Journal, Vol. 11, Issue 5
  • DOI: 10.1038/ismej.2016.191

Versatile and open software for comparing large genomes
journal, January 2004

  • Kurtz, Stefan; Phillippy, Adam; Delcher, Arthur L.
  • Genome Biology, Vol. 5, Issue 2, R12
  • DOI: 10.1186/gb-2004-5-2-r12

Modified Pathway To Synthesize Ribulose 1,5-Bisphosphate in Methanogenic Archaea
journal, September 2004


Global extent, development and economic impact of acid soils
journal, April 1995

  • von Uexküll, H. R.; Mutert, E.
  • Plant and Soil, Vol. 171, Issue 1
  • DOI: 10.1007/BF00009558

Shifting the genomic gold standard for the prokaryotic species definition
journal, October 2009

  • Richter, Michael; Rosselló-Móra, Ramon
  • Proceedings of the National Academy of Sciences, Vol. 106, Issue 45
  • DOI: 10.1073/pnas.0906412106

Archaea produce lower yields of N 2 O than bacteria during aerobic ammonia oxidation in soil : N
journal, April 2016

  • Hink, Linda; Nicol, Graeme W.; Prosser, James I.
  • Environmental Microbiology, Vol. 19, Issue 12
  • DOI: 10.1111/1462-2920.13282

A Monocarboxylate Permease of Rhizobium leguminosarum Is the First Member of a New Subfamily of Transporters
journal, October 2002


PhyloBayes 3: a Bayesian software package for phylogenetic reconstruction and molecular dating
journal, June 2009


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

Mauve: Multiple Alignment of Conserved Genomic Sequence With Rearrangements
journal, June 2004


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

Archaeal Type III RuBisCOs Function in a Pathway for AMP Metabolism
journal, February 2007


GET_HOMOLOGUES, a Versatile Software Package for Scalable and Robust Microbial Pangenome Analysis
journal, October 2013

  • Contreras-Moreira, Bruno; Vinuesa, Pablo
  • Applied and Environmental Microbiology, Vol. 79, Issue 24
  • DOI: 10.1128/AEM.02411-13

Controls on Nitrogen Cycling in Terrestrial Ecosystems: a Synthetic Analysis of Literature data
journal, May 2005

  • Booth, Mary S.; Stark, John M.; Rastetter, Edward
  • Ecological Monographs, Vol. 75, Issue 2
  • DOI: 10.1890/04-0988

MicroScope: a platform for microbial genome annotation and comparative genomics
journal, January 2009


A Mesophilic, Autotrophic, Ammonia-Oxidizing Archaeon of Thaumarchaeal Group I.1a Cultivated from a Deep Oligotrophic Soil Horizon
journal, April 2014

  • Jung, Man-Young; Park, Soo-Je; Kim, So-Jeong
  • Applied and Environmental Microbiology, Vol. 80, Issue 12
  • DOI: 10.1128/AEM.03730-13

Natural products containing a diazo group
journal, January 2011

  • Nawrat, Christopher C.; Moody, Christopher J.
  • Natural Product Reports, Vol. 28, Issue 8
  • DOI: 10.1039/c1np00031d

Uniting the classification of cultured and uncultured bacteria and archaea using 16S rRNA gene sequences
journal, August 2014

  • Yarza, Pablo; Yilmaz, Pelin; Pruesse, Elmar
  • Nature Reviews Microbiology, Vol. 12, Issue 9
  • DOI: 10.1038/nrmicro3330

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

Reaction mechanism of azoreductases suggests convergent evolution with quinone oxidoreductases
journal, August 2010


Prodigal: prokaryotic gene recognition and translation initiation site identification
journal, March 2010


Genome analysis of multiple pathogenic isolates of Streptococcus agalactiae: Implications for the microbial "pan-genome"
journal, September 2005

  • Tettelin, H.; Masignani, V.; Cieslewicz, M. J.
  • Proceedings of the National Academy of Sciences, Vol. 102, Issue 39
  • DOI: 10.1073/pnas.0506758102

MyTaxa: an advanced taxonomic classifier for genomic and metagenomic sequences
journal, March 2014

  • Luo, Chengwei; Rodriguez-R, Luis M.; Konstantinidis, Konstantinos T.
  • Nucleic Acids Research, Vol. 42, Issue 8
  • DOI: 10.1093/nar/gku169

Nitrogen in Agriculture: Balancing the Cost of an Essential Resource
journal, November 2009


Microbial species delineation using whole genome sequences
journal, July 2015

  • Varghese, Neha J.; Mukherjee, Supratim; Ivanova, Natalia
  • Nucleic Acids Research, Vol. 43, Issue 14
  • DOI: 10.1093/nar/gkv657

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

Alkaline pH homeostasis in bacteria: New insights
journal, November 2005

  • Padan, Etana; Bibi, Eitan; Ito, Masahiro
  • Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 1717, Issue 2
  • DOI: 10.1016/j.bbamem.2005.09.010

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

The Divergent AmoC3 Subunit of Ammonia Monooxygenase Functions as Part of a Stress Response System in Nitrosomonas europaea
journal, April 2012

  • Berube, P. M.; Stahl, D. A.
  • Journal of Bacteriology, Vol. 194, Issue 13
  • DOI: 10.1128/JB.00133-12

OrthoMCL: Identification of Ortholog Groups for Eukaryotic Genomes
journal, September 2003


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

Search and clustering orders of magnitude faster than BLAST
journal, August 2010


Phylogenetic congruence and ecological coherence in terrestrial Thaumarchaeota
journal, July 2015

  • Oton, Eduard Vico; Quince, Christopher; Nicol, Graeme W.
  • The ISME Journal, Vol. 10, Issue 1
  • DOI: 10.1038/ismej.2015.101

Proteomics and comparative genomics of Nitrososphaera viennensis reveal the core genome and adaptations of archaeal ammonia oxidizers
journal, November 2016

  • Kerou, Melina; Offre, Pierre; Valledor, Luis
  • Proceedings of the National Academy of Sciences, Vol. 113, Issue 49
  • DOI: 10.1073/pnas.1601212113

Conserved active site cysteine residue of archaeal THI4 homolog is essential for thiamine biosynthesis in Haloferax volcanii
journal, October 2014


Characterization of probiotic Escherichia coli isolates with a novel pan-genome microarray
journal, January 2007


Variability of the transporter gene complement in ammonia-oxidizing archaea
journal, December 2014


Comparative Genomics of Candidate Phylum TM6 Suggests That Parasitism Is Widespread and Ancestral in This Lineage
journal, November 2015

  • Yeoh, Yun Kit; Sekiguchi, Yuji; Parks, Donovan H.
  • Molecular Biology and Evolution, Vol. 33, Issue 4
  • DOI: 10.1093/molbev/msv281

Characterisation of terrestrial acidophilic archaeal ammonia oxidisers and their inhibition and stimulation by organic compounds
journal, July 2014

  • Lehtovirta-Morley, Laura E.; Ge, Chaorong; Ross, Jenna
  • FEMS Microbiology Ecology, Vol. 89, Issue 3
  • DOI: 10.1111/1574-6941.12353

SPAdes: A New Genome Assembly Algorithm and Its Applications to Single-Cell Sequencing
journal, May 2012

  • Bankevich, Anton; Nurk, Sergey; Antipov, Dmitry
  • Journal of Computational Biology, Vol. 19, Issue 5
  • DOI: 10.1089/cmb.2012.0021

Emergent Macrophytes Act Selectively on Ammonia-Oxidizing Bacteria and Archaea
journal, June 2012

  • Trias, Rosalia; Ruiz-Rueda, Olaya; García-Lledó, Arantzazu
  • Applied and Environmental Microbiology, Vol. 78, Issue 17
  • DOI: 10.1128/AEM.00919-12

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


Genome sequences of rare, uncultured bacteria obtained by differential coverage binning of multiple metagenomes
journal, May 2013

  • Albertsen, Mads; Hugenholtz, Philip; Skarshewski, Adam
  • Nature Biotechnology, Vol. 31, Issue 6
  • DOI: 10.1038/nbt.2579

Mobility and Bioavailability of Heavy Metals and Metalloids in soil Environments
journal, January 2010


Keeping It Simple, Transport Mechanism and pH Regulation in Na + /H + Exchangers
journal, March 2014

  • Călinescu, Octavian; Paulino, Cristina; Kühlbrandt, Werner
  • Journal of Biological Chemistry, Vol. 289, Issue 19
  • DOI: 10.1074/jbc.M113.542993

Molecular adaptation of ammonia monooxygenase during independent pH specialization in Thaumarchaeota
journal, March 2016

  • Macqueen, Daniel J.; Gubry-Rangin, Cécile
  • Molecular Ecology, Vol. 25, Issue 9
  • DOI: 10.1111/mec.13607

Consortia of low-abundance bacteria drive sulfate reduction-dependent degradation of fermentation products in peat soil microcosms
journal, March 2016

  • Hausmann, Bela; Knorr, Klaus-Holger; Schreck, Katharina
  • The ISME Journal, Vol. 10, Issue 10
  • DOI: 10.1038/ismej.2016.42

Biochemical Characterization of the C4-Dicarboxylate Transporter DctA from Bacillus subtilis
journal, April 2010

  • Groeneveld, M.; Detert Oude Weme, R. G. J.; Duurkens, R. H.
  • Journal of Bacteriology, Vol. 192, Issue 11
  • DOI: 10.1128/JB.00136-10

Contributions of ammonia-oxidizing archaea and bacteria to nitrification in Oregon forest soils
journal, June 2015


Life in acid: pH homeostasis in acidophiles
journal, April 2007


The sodium/substrate symporter family: structural and functional features
journal, August 2002


SOAPdenovo2: an empirically improved memory-efficient short-read de novo assembler
journal, December 2012


Predominance of thaumarchaeal ammonia oxidizer abundance and transcriptional activity in an acidic fen: Ammonia oxidizers in an acidic fen
journal, September 2012


Identifying Potential Mechanisms Enabling Acidophily in the Ammonia-Oxidizing Archaeon “Candidatus Nitrosotalea devanaterra”
journal, February 2016

  • Lehtovirta-Morley, Laura E.; Sayavedra-Soto, Luis A.; Gallois, Nicolas
  • Applied and Environmental Microbiology, Vol. 82, Issue 9
  • DOI: 10.1128/AEM.04031-15

Thermoplasmatales
book, January 2006


FastTree: Computing Large Minimum Evolution Trees with Profiles instead of a Distance Matrix
journal, April 2009

  • Price, M. N.; Dehal, P. S.; Arkin, A. P.
  • Molecular Biology and Evolution, Vol. 26, Issue 7
  • DOI: 10.1093/molbev/msp077

Insights into the phylogeny and coding potential of microbial dark matter
journal, July 2013

  • Rinke, Christian; Schwientek, Patrick; Sczyrba, Alexander
  • Nature, Vol. 499, Issue 7459
  • DOI: 10.1038/nature12352

Putative ACP Phosphodiesterase Gene ( acpD ) Encodes an Azoreductase
journal, October 2001

  • Nakanishi, Masayuki; Yatome, Chizuko; Ishida, Norihisa
  • Journal of Biological Chemistry, Vol. 276, Issue 49
  • DOI: 10.1074/jbc.M104483200

Using RAxML to Infer Phylogenies
journal, September 2015


NhaA Na+/H+ Antiporter Mutants That Hardly React to the Membrane Potential
journal, April 2014


Niche specialization of terrestrial archaeal ammonia oxidizers
journal, December 2011

  • Gubry-Rangin, C.; Hai, B.; Quince, C.
  • Proceedings of the National Academy of Sciences, Vol. 108, Issue 52
  • DOI: 10.1073/pnas.1109000108

Physiological and genomic characterization of two novel marine thaumarchaeal strains indicates niche differentiation
journal, November 2015


DNA–DNA hybridization values and their relationship to whole-genome sequence similarities
journal, January 2007

  • Klappenbach, Joel A.; Goris, Johan; Vandamme, Peter
  • International Journal of Systematic and Evolutionary Microbiology, Vol. 57, Issue 1
  • DOI: 10.1099/ijs.0.64483-0

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