Hydrogen peroxide detoxification is a key mechanism for growth of ammonia-oxidizing archaea

Jong-Geol Kim, Soo-Je Park, Jaap S. Sinninghe Damsté, Stefan Schouten, W. Irene C. Rijpstra, Man-Young Jung, So-Jeong Kim, Joo-Han Gwak, Heeji Hong, Ok-Ja Si, Sanghoon Lee, Eugene L. Madsen, Sung-Keun Rhee

Research output: Contribution to journalArticleAcademicpeer-review

Abstract

Ammonia-oxidizing archaea (AOA), that is, members of the Thaumarchaeota phylum, occur ubiquitously in the environment and are of major significance for global nitrogen cycling. However, controls on cell growth and organic carbon assimilation by AOA are poorly understood. We isolated an ammonia-oxidizing archaeon (designated strain DDS1) from seawater and used this organism to study the physiology of ammonia oxidation. These findings were confirmed using four additional Thaumarchaeota strains from both marine and terrestrial habitats. Ammonia oxidation by strain DDS1 was enhanced in coculture with other bacteria, as well as in artificial seawater media supplemented with α-keto acids (e.g., pyruvate, oxaloacetate). α-Keto acid-enhanced activity of AOA has previously been interpreted as evidence of mixotrophy. However, assays for heterotrophic growth indicated that incorporation of pyruvate into archaeal membrane lipids was negligible. Lipid carbon atoms were, instead, derived from dissolved inorganic carbon, indicating strict autotrophic growth. α-Keto acids spontaneously detoxify H2O2 via a nonenzymatic decarboxylation reaction, suggesting a role of α-keto acids as H2O2 scavengers. Indeed, agents that also scavenge H2O2, such as dimethylthiourea and catalase, replaced the α-keto acid requirement, enhancing growth of strain DDS1. In fact, in the absence of α-keto acids, strain DDS1 and other AOA isolates were shown to endogenously produce H2O2 (up to ∼4.5 μM), which was inhibitory to growth. Genomic analyses indicated catalase genes are largely absent in the AOA. Our results indicate that AOA broadly feature strict autotrophic nutrition and implicate H2O2 as an important factor determining the activity, evolution, and community ecology of AOA ecotypes.
Original languageEnglish
Pages (from-to)7888-7893
Number of pages6
JournalProceedings of the National Academy of Sciences of the United States of America
Volume113
Issue number28
DOIs
Publication statusPublished - 12 Jul 2016

Keywords

  • Ammonia-oxidizing archaea
  • H2O2 detoxification
  • Mixotrophy
  • α-keto acid
  • 2 oxoacid
  • ammonia
  • carbon
  • catalase
  • dimethylthiourea
  • hydrogen peroxide
  • membrane lipid
  • peroxidase
  • pyruvic acid
  • reactive oxygen metabolite
  • sea water
  • ammonia oxidizing archaeon
  • article
  • autotrophy
  • bacterial growth
  • carbon source
  • detoxification
  • enzyme activity
  • marine environment
  • mixotrophy
  • nonhuman
  • oxidation
  • priority journal

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