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

Graeme W Nicol, Sven Leininger, Christa Schleper, James I Prosser

Research output: Contribution to journalArticle

754 Citations (Scopus)

Abstract

Autotrophic ammonia oxidation occurs in acid soils, even though laboratory cultures of isolated ammonia oxidizing bacteria fail to grow below neutral pH. To investigate whether archaea possessing ammonia monooxygenase genes were responsible for autotrophic nitrification in acid soils, the community structure and phylogeny of ammonia oxidizing bacteria and archaea were determined across a soil pH gradient (4.9-7.5) by amplifying 16S rRNA and amoA genes followed by denaturing gradient gel electrophoresis (DGGE) and sequence analysis. The structure of both communities changed with soil pH, with distinct populations in acid and neutral soils. Phylogenetic reconstructions of crenarchaeal 16S rRNA and amoA genes confirmed selection of distinct lineages within the pH gradient and high similarity in phylogenies indicated a high level of congruence between 16S rRNA and amoA genes. The abundance of archaeal and bacterial amoA gene copies and mRNA transcripts contrasted across the pH gradient. Archaeal amoA gene and transcript abundance decreased with increasing soil pH, while bacterial amoA gene abundance was generally lower and transcripts increased with increasing pH. Short-term activity was investigated by DGGE analysis of gene transcripts in microcosms containing acidic or neutral soil or mixed soil with pH readjusted to that of native soils. Although mixed soil microcosms contained identical archaeal ammonia oxidizer communities, those adapted to acidic or neutral pH ranges showed greater relative activity at their native soil pH. Findings indicate that different bacterial and archaeal ammonia oxidizer phylotypes are selected in soils of different pH and that these differences in community structure and abundances are reflected in different contributions to ammonia oxidizer activity. They also suggest that both groups of ammonia oxidizers have distinct physiological characteristics and ecological niches, with consequences for nitrification in acid soils.
Original languageEnglish
Pages (from-to)2966-2978
Number of pages13
JournalEnvironmental Microbiology
Volume10
Issue number11
Early online date14 Aug 2008
DOIs
Publication statusPublished - Nov 2008

Fingerprint

Archaea
Ammonia
soil pH
ammonia
Soil
Bacteria
bacterium
bacteria
oxidants
gene
genes
soil
acid soils
acid soil
community structure
Proton-Motive Force
ribosomal RNA
denaturing gradient gel electrophoresis
nitrification
rRNA Genes

Keywords

  • Ammonia
  • Archaeal Proteins
  • Bacteria
  • Bacterial Physiological Phenomena
  • Bacterial Proteins
  • Biodiversity
  • Cluster Analysis
  • Crenarchaeota
  • DNA Fingerprinting
  • Electrophoresis, Polyacrylamide Gel
  • Hydrogen-Ion Concentration
  • Molecular Sequence Data
  • Nitrites
  • Nucleic Acid Denaturation
  • Oxidation-Reduction
  • Oxidoreductases
  • RNA, Archaeal
  • RNA, Bacterial
  • RNA, Ribosomal, 16S
  • Sequence Analysis, DNA
  • Soil Microbiology
  • Transcription, Genetic

Cite this

The influence of soil pH on the diversity, abundance and transcriptional activity of ammonia oxidizing archaea and bacteria. / Nicol, Graeme W; Leininger, Sven; Schleper, Christa; Prosser, James I.

In: Environmental Microbiology, Vol. 10, No. 11, 11.2008, p. 2966-2978.

Research output: Contribution to journalArticle

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T1 - The influence of soil pH on the diversity, abundance and transcriptional activity of ammonia oxidizing archaea and bacteria

AU - Nicol, Graeme W

AU - Leininger, Sven

AU - Schleper, Christa

AU - Prosser, James I

PY - 2008/11

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N2 - Autotrophic ammonia oxidation occurs in acid soils, even though laboratory cultures of isolated ammonia oxidizing bacteria fail to grow below neutral pH. To investigate whether archaea possessing ammonia monooxygenase genes were responsible for autotrophic nitrification in acid soils, the community structure and phylogeny of ammonia oxidizing bacteria and archaea were determined across a soil pH gradient (4.9-7.5) by amplifying 16S rRNA and amoA genes followed by denaturing gradient gel electrophoresis (DGGE) and sequence analysis. The structure of both communities changed with soil pH, with distinct populations in acid and neutral soils. Phylogenetic reconstructions of crenarchaeal 16S rRNA and amoA genes confirmed selection of distinct lineages within the pH gradient and high similarity in phylogenies indicated a high level of congruence between 16S rRNA and amoA genes. The abundance of archaeal and bacterial amoA gene copies and mRNA transcripts contrasted across the pH gradient. Archaeal amoA gene and transcript abundance decreased with increasing soil pH, while bacterial amoA gene abundance was generally lower and transcripts increased with increasing pH. Short-term activity was investigated by DGGE analysis of gene transcripts in microcosms containing acidic or neutral soil or mixed soil with pH readjusted to that of native soils. Although mixed soil microcosms contained identical archaeal ammonia oxidizer communities, those adapted to acidic or neutral pH ranges showed greater relative activity at their native soil pH. Findings indicate that different bacterial and archaeal ammonia oxidizer phylotypes are selected in soils of different pH and that these differences in community structure and abundances are reflected in different contributions to ammonia oxidizer activity. They also suggest that both groups of ammonia oxidizers have distinct physiological characteristics and ecological niches, with consequences for nitrification in acid soils.

AB - Autotrophic ammonia oxidation occurs in acid soils, even though laboratory cultures of isolated ammonia oxidizing bacteria fail to grow below neutral pH. To investigate whether archaea possessing ammonia monooxygenase genes were responsible for autotrophic nitrification in acid soils, the community structure and phylogeny of ammonia oxidizing bacteria and archaea were determined across a soil pH gradient (4.9-7.5) by amplifying 16S rRNA and amoA genes followed by denaturing gradient gel electrophoresis (DGGE) and sequence analysis. The structure of both communities changed with soil pH, with distinct populations in acid and neutral soils. Phylogenetic reconstructions of crenarchaeal 16S rRNA and amoA genes confirmed selection of distinct lineages within the pH gradient and high similarity in phylogenies indicated a high level of congruence between 16S rRNA and amoA genes. The abundance of archaeal and bacterial amoA gene copies and mRNA transcripts contrasted across the pH gradient. Archaeal amoA gene and transcript abundance decreased with increasing soil pH, while bacterial amoA gene abundance was generally lower and transcripts increased with increasing pH. Short-term activity was investigated by DGGE analysis of gene transcripts in microcosms containing acidic or neutral soil or mixed soil with pH readjusted to that of native soils. Although mixed soil microcosms contained identical archaeal ammonia oxidizer communities, those adapted to acidic or neutral pH ranges showed greater relative activity at their native soil pH. Findings indicate that different bacterial and archaeal ammonia oxidizer phylotypes are selected in soils of different pH and that these differences in community structure and abundances are reflected in different contributions to ammonia oxidizer activity. They also suggest that both groups of ammonia oxidizers have distinct physiological characteristics and ecological niches, with consequences for nitrification in acid soils.

KW - Ammonia

KW - Archaeal Proteins

KW - Bacteria

KW - Bacterial Physiological Phenomena

KW - Bacterial Proteins

KW - Biodiversity

KW - Cluster Analysis

KW - Crenarchaeota

KW - DNA Fingerprinting

KW - Electrophoresis, Polyacrylamide Gel

KW - Hydrogen-Ion Concentration

KW - Molecular Sequence Data

KW - Nitrites

KW - Nucleic Acid Denaturation

KW - Oxidation-Reduction

KW - Oxidoreductases

KW - RNA, Archaeal

KW - RNA, Bacterial

KW - RNA, Ribosomal, 16S

KW - Sequence Analysis, DNA

KW - Soil Microbiology

KW - Transcription, Genetic

U2 - 10.1111/j.1462-2920.2008.01701.x

DO - 10.1111/j.1462-2920.2008.01701.x

M3 - Article

C2 - 18707610

VL - 10

SP - 2966

EP - 2978

JO - Environmental Microbiology

JF - Environmental Microbiology

SN - 1462-2912

IS - 11

ER -