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

Craig W. Herbold, Laura E. Lehtovirta-Morley, Man-Young Jung, Nico Jehmlich, Bela Hausmann, Ping Han, Alexander Loy, Michael Pester, Luis A. Sayavedra-Soto, Sung-Keun Rhee, James I. Prosser, Graeme W. Nicol, Michael Wagner, Cecile Gubry-Rangin

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Abstract

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 are not closely related to each other and 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. Interestingly, phylogenetic analyses of four of these core gene families clearly showed their acquisition by the Ca. Nitrosotalea common ancestor via horizontal gene transfer from Euryarchaeota of the order Thermoplasmatales. This order comprises acidophiles growing preferentially below pH 2 and, given the potential functional involvement in low pH adaptation of some of these laterally acquired genes, we hypothesize that gene exchange with these acidophiles contributed to the competitive success of the Ca. Nitrosotalea lineage in acidic environments.
Original languageEnglish
Pages (from-to)4939-4952
Number of pages14
JournalEnvironmental Microbiology
Volume19
Issue number12
Early online date4 Dec 2017
DOIs
Publication statusPublished - Dec 2017

Fingerprint

Archaea
Genomics
Ammonia
genomics
ammonia
genome
Genome
gene
genes
Genes
Thermoplasmales
Euryarchaeota
Metagenome
Physiological Adaptation
Nitrification
Horizontal Gene Transfer
proteomics
gene transfer
fens
fen

Keywords

  • archaea
  • element cycles and biogeochemical processes
  • environmental genomics
  • evolution/evolutionary processes/gene transfer/mutation
  • genomics/functional genomics/comparative genomics

Cite this

Herbold, C. W., Lehtovirta-Morley, L. E., Jung, M-Y., Jehmlich, N., Hausmann, B., Han, P., ... Gubry-Rangin, C. (2017). Ammonia-oxidising archaea living at low pH: Insights from comparative genomics. Environmental Microbiology, 19(12), 4939-4952. https://doi.org/10.1111/1462-2920.13971

Ammonia-oxidising archaea living at low pH : Insights from comparative genomics. / 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, Cecile.

In: Environmental Microbiology, Vol. 19, No. 12, 12.2017, p. 4939-4952.

Research output: Contribution to journalArticle

Herbold, CW, Lehtovirta-Morley, LE, Jung, M-Y, Jehmlich, N, Hausmann, B, Han, P, Loy, A, Pester, M, Sayavedra-Soto, LA, Rhee, S-K, Prosser, JI, Nicol, GW, Wagner, M & Gubry-Rangin, C 2017, 'Ammonia-oxidising archaea living at low pH: Insights from comparative genomics', Environmental Microbiology, vol. 19, no. 12, pp. 4939-4952. https://doi.org/10.1111/1462-2920.13971
Herbold CW, Lehtovirta-Morley LE, Jung M-Y, Jehmlich N, Hausmann B, Han P et al. Ammonia-oxidising archaea living at low pH: Insights from comparative genomics. Environmental Microbiology. 2017 Dec;19(12):4939-4952. 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 ; Gubry-Rangin, Cecile. / Ammonia-oxidising archaea living at low pH : Insights from comparative genomics. In: Environmental Microbiology. 2017 ; Vol. 19, No. 12. pp. 4939-4952.
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abstract = "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 are not closely related to each other and 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. Interestingly, phylogenetic analyses of four of these core gene families clearly showed their acquisition by the Ca. Nitrosotalea common ancestor via horizontal gene transfer from Euryarchaeota of the order Thermoplasmatales. This order comprises acidophiles growing preferentially below pH 2 and, given the potential functional involvement in low pH adaptation of some of these laterally acquired genes, we hypothesize that gene exchange with these acidophiles contributed to the competitive success of the Ca. Nitrosotalea lineage in acidic environments.",
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author = "Herbold, {Craig W.} and Lehtovirta-Morley, {Laura E.} and Man-Young Jung and Nico Jehmlich and Bela Hausmann and Ping Han and Alexander Loy and Michael Pester and Sayavedra-Soto, {Luis A.} and Sung-Keun Rhee and Prosser, {James I.} and Nicol, {Graeme W.} and Michael Wagner and Cecile Gubry-Rangin",
note = "MW and CWH were supported by an ERC Advanced Grant (NITRICARE, 294343), CGR by a Natural Environment Research Council (NERC) Fellowship (NE/J019151/1), a NERC Standard Grant (NE/K016342/1) and a Royal Society University Research Fellowship (UF150571) and LEL-M by a NERC standard grant (NE/I027835/1) and a Royal Society Dorothy Hodgkin Research Fellowship (DH150187). GN was funded by the AXA Research Fund. AL and BH were supported by the Austrian Science Fund (FWF, P23117-B17). We thank the staff of the Joint Genome Institute (CSP605, supported by the Office of Science of the US Department of Energy under Contract No. DE-AC02-05CH11231) and Ulrich Stingl for metagenome and metatranscriptome sequencing of Schl{\"o}ppnerbrunnen peat soil and Mads Albertsen, Per Halkj{\ae}r Nielsen, Thomas Rattei, and Tony Travis for bioinformatics support.",
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AU - Herbold, Craig W.

AU - Lehtovirta-Morley, Laura E.

AU - Jung, Man-Young

AU - Jehmlich, Nico

AU - Hausmann, Bela

AU - Han, Ping

AU - Loy, Alexander

AU - Pester, Michael

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N1 - MW and CWH were supported by an ERC Advanced Grant (NITRICARE, 294343), CGR by a Natural Environment Research Council (NERC) Fellowship (NE/J019151/1), a NERC Standard Grant (NE/K016342/1) and a Royal Society University Research Fellowship (UF150571) and LEL-M by a NERC standard grant (NE/I027835/1) and a Royal Society Dorothy Hodgkin Research Fellowship (DH150187). GN was funded by the AXA Research Fund. AL and BH were supported by the Austrian Science Fund (FWF, P23117-B17). We thank the staff of the Joint Genome Institute (CSP605, supported by the Office of Science of the US Department of Energy under Contract No. DE-AC02-05CH11231) and Ulrich Stingl for metagenome and metatranscriptome sequencing of Schlöppnerbrunnen peat soil and Mads Albertsen, Per Halkjær Nielsen, Thomas Rattei, and Tony Travis for bioinformatics support.

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KW - element cycles and biogeochemical processes

KW - environmental genomics

KW - evolution/evolutionary processes/gene transfer/mutation

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