Autotrophic ammonia oxidation by soil thaumarchaea

Li-Mei Zhang, Pierre R Offre, Ji-Zheng He, Daniel T Verhamme, Graeme W Nicol, James I Prosser

Research output: Contribution to journalArticlepeer-review

244 Citations (Scopus)

Abstract

Nitrification plays a central role in the global nitrogen cycle and is responsible for significant losses of nitrogen fertilizer, atmospheric pollution by the greenhouse gas nitrous oxide, and nitrate pollution of groundwaters. Ammonia oxidation, the first step in nitrification, was thought to be performed by autotrophic bacteria until the recent discovery of archaeal ammonia oxidizers. Autotrophic archaeal ammonia oxidizers have been cultivated from marine and thermal spring environments, but the relative importance of bacteria and archaea in soil nitrification is unclear and it is believed that soil archaeal ammonia oxidizers may use organic carbon, rather than growing autotrophically. In this soil microcosm study, stable isotope probing was used to demonstrate incorporation of (13)C-enriched carbon dioxide into the genomes of thaumarchaea possessing two functional genes: amoA, encoding a subunit of ammonia monooxygenase that catalyses the first step in ammonia oxidation; and hcd, a key gene in the autotrophic 3-hydroxypropionate/4-hydroxybutyrate cycle, which has been found so far only in archaea. Nitrification was accompanied by increases in archaeal amoA gene abundance and changes in amoA gene diversity, but no change was observed in bacterial amoA genes. Archaeal, but not bacterial, amoA genes were also detected in (13)C-labeled DNA, demonstrating inorganic CO(2) fixation by archaeal, but not bacterial, ammonia oxidizers. Autotrophic archaeal ammonia oxidation was further supported by coordinate increases in amoA and hcd gene abundance in (13)C-labeled DNA. The results therefore provide direct evidence for a role for archaea in soil ammonia oxidation and demonstrate autotrophic growth of ammonia oxidizing archaea in soil.
Original languageEnglish
Pages (from-to)17240-17245
Number of pages6
JournalPNAS
Volume107
Issue number40
Early online date20 Sep 2010
DOIs
Publication statusPublished - 5 Oct 2010

Keywords

  • ammonia oxidizers
  • nitrification
  • soil
  • autotrophy
  • stable isotope probing

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