Niche specialization of terrestrial archaeal ammonia oxidizers

Cecile Gubry-Rangin, Brigitte Hai, Christopher Quince, Marion Engel, Bruce C. Thomson, Phillip James, Michael Schloter, Robert I. Griffiths, James I. Prosser, Graeme W. Nicol

Research output: Contribution to journalArticle

217 Citations (Scopus)

Abstract

Soil pH is a major determinant of microbial ecosystem processes and potentially a major driver of evolution, adaptation, and diversity of ammonia oxidizers, which control soil nitrification. Archaea are major components of soil microbial communities and contribute significantly to ammonia oxidation in some soils. To determine whether pH drives evolutionary adaptation and community structure of soil archaeal ammonia oxidizers, sequences of amoA, a key functional gene of ammonia oxidation, were examined in soils at global, regional, and local scales. Globally distributed database sequences clustered into 18 well-supported phylogenetic lineages that dominated specific soil pH ranges classified as acidic (pH < 5), acido-neutral (5 <= pH < 7), or alkalinophilic (pH >= 7). To determine whether patterns were reproduced at regional and local scales, amoA gene fragments were amplified from DNA extracted from 47 soils in the United Kingdom (pH 3.5-8.7), including a pH-gradient formed by seven soils at a single site (pH 4.5-7.5). High-throughput sequencing and analysis of amoA gene fragments identified an additional, previously undiscovered phylogenetic lineage and revealed similar pH-associated distribution patterns at global, regional, and local scales, which were most evident for the five most abundant clusters. Archaeal amoA abundance and diversity increased with soil pH, which was the only physicochemical characteristic measured that significantly influenced community structure. These results suggest evolution based on specific adaptations to soil pH and niche specialization, resulting in a global distribution of archaeal lineages that have important consequences for soil ecosystem function and nitrogen cycling.

Original languageEnglish
Pages (from-to)21206-21211
Number of pages6
JournalPNAS
Volume108
Issue number52
Early online date8 Dec 2011
DOIs
Publication statusPublished - 27 Dec 2011

Keywords

  • Thaumarchaeota
  • Nitrosotalea devanaterra
  • 454 pyrosequencing
  • Bacterial communities
  • Low PH
  • Mesophilic crenarchaeota
  • Soil-PH
  • Oxidation
  • Diversity
  • Nitrification
  • Biogeography
  • Populations
  • Cultivation

Cite this

Gubry-Rangin, C., Hai, B., Quince, C., Engel, M., Thomson, B. C., James, P., ... Nicol, G. W. (2011). Niche specialization of terrestrial archaeal ammonia oxidizers. PNAS, 108(52), 21206-21211. https://doi.org/10.1073/pnas.1109000108

Niche specialization of terrestrial archaeal ammonia oxidizers. / Gubry-Rangin, Cecile; Hai, Brigitte; Quince, Christopher; Engel, Marion; Thomson, Bruce C.; James, Phillip; Schloter, Michael; Griffiths, Robert I.; Prosser, James I.; Nicol, Graeme W.

In: PNAS, Vol. 108, No. 52, 27.12.2011, p. 21206-21211.

Research output: Contribution to journalArticle

Gubry-Rangin, C, Hai, B, Quince, C, Engel, M, Thomson, BC, James, P, Schloter, M, Griffiths, RI, Prosser, JI & Nicol, GW 2011, 'Niche specialization of terrestrial archaeal ammonia oxidizers' PNAS, vol. 108, no. 52, pp. 21206-21211. https://doi.org/10.1073/pnas.1109000108
Gubry-Rangin C, Hai B, Quince C, Engel M, Thomson BC, James P et al. Niche specialization of terrestrial archaeal ammonia oxidizers. PNAS. 2011 Dec 27;108(52):21206-21211. https://doi.org/10.1073/pnas.1109000108
Gubry-Rangin, Cecile ; Hai, Brigitte ; Quince, Christopher ; Engel, Marion ; Thomson, Bruce C. ; James, Phillip ; Schloter, Michael ; Griffiths, Robert I. ; Prosser, James I. ; Nicol, Graeme W. / Niche specialization of terrestrial archaeal ammonia oxidizers. In: PNAS. 2011 ; Vol. 108, No. 52. pp. 21206-21211.
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AU - Hai, Brigitte

AU - Quince, Christopher

AU - Engel, Marion

AU - Thomson, Bruce C.

AU - James, Phillip

AU - Schloter, Michael

AU - Griffiths, Robert I.

AU - Prosser, James I.

AU - Nicol, Graeme W.

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AB - Soil pH is a major determinant of microbial ecosystem processes and potentially a major driver of evolution, adaptation, and diversity of ammonia oxidizers, which control soil nitrification. Archaea are major components of soil microbial communities and contribute significantly to ammonia oxidation in some soils. To determine whether pH drives evolutionary adaptation and community structure of soil archaeal ammonia oxidizers, sequences of amoA, a key functional gene of ammonia oxidation, were examined in soils at global, regional, and local scales. Globally distributed database sequences clustered into 18 well-supported phylogenetic lineages that dominated specific soil pH ranges classified as acidic (pH < 5), acido-neutral (5 <= pH < 7), or alkalinophilic (pH >= 7). To determine whether patterns were reproduced at regional and local scales, amoA gene fragments were amplified from DNA extracted from 47 soils in the United Kingdom (pH 3.5-8.7), including a pH-gradient formed by seven soils at a single site (pH 4.5-7.5). High-throughput sequencing and analysis of amoA gene fragments identified an additional, previously undiscovered phylogenetic lineage and revealed similar pH-associated distribution patterns at global, regional, and local scales, which were most evident for the five most abundant clusters. Archaeal amoA abundance and diversity increased with soil pH, which was the only physicochemical characteristic measured that significantly influenced community structure. These results suggest evolution based on specific adaptations to soil pH and niche specialization, resulting in a global distribution of archaeal lineages that have important consequences for soil ecosystem function and nitrogen cycling.

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KW - Diversity

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KW - Biogeography

KW - Populations

KW - Cultivation

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