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

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 ?-keto acids (e.g., pyruvate, oxaloacetate). ?-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. ?-Keto acids spontaneously detoxify H2O2 via a nonenzymatic decarboxylation reaction, suggesting a role of ?-keto acids as H2O2 scavengers. Indeed, agents that also scavenge H2O2, such as dimethylthiourea and catalase, replaced the ?-keto acid requirement, enhancing growth of strain DDS1. In fact, in the absence of ?-keto acids, strain DDS1 and other AOA isolates were shown to endogenously produce H2O2 (up to ?4.5 ?M), 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.

SUBMITTER: Kim JG

PROVIDER: S-EPMC4948306 | biostudies-literature | 2016 Jul

REPOSITORIES: biostudies-literature

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

Kim Jong-Geol JG Park Soo-Je SJ Sinninghe Damsté Jaap S JS Schouten Stefan S Rijpstra W Irene C WI Jung Man-Young MY Kim So-Jeong SJ Gwak Joo-Han JH Hong Heeji H Si Ok-Ja OJ Lee SangHoon S Madsen Eugene L EL Rhee Sung-Keun SK

Proceedings of the National Academy of Sciences of the United States of America 20160623 28

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 fro ...[more]

PMID: 27339136

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Project description:BackgroundThe global distribution of ammonia-oxidizing archaea (AOA), which play a pivotal role in the nitrification process, has been confirmed through numerous ecological studies. Though newly available amoA (ammonia monooxygenase subunit A) gene sequences from new environments are accumulating rapidly in public repositories, a lack of information on the ecological and evolutionary factors shaping community assembly of AOA on the global scale is apparent.Methodology and resultsWe conducted a meta-analysis on uncultured AOA using over ca. 6,200 archaeal amoA gene sequences, so as to reveal their community distribution patterns along a wide spectrum of physicochemical conditions and habitat types. The sequences were dereplicated at 95% identity level resulting in a dataset containing 1,476 archaeal amoA gene sequences from eight habitat types: namely soil, freshwater, freshwater sediment, estuarine sediment, marine water, marine sediment, geothermal system, and symbiosis. The updated comprehensive amoA phylogeny was composed of three major monophyletic clusters (i.e. Nitrosopumilus, Nitrosotalea, Nitrosocaldus) and a non-monophyletic cluster constituted mostly by soil and sediment sequences that we named Nitrososphaera. Diversity measurements indicated that marine and estuarine sediments as well as symbionts might be the largest reservoirs of AOA diversity. Phylogenetic analyses were further carried out using macroevolutionary analyses to explore the diversification pattern and rates of nitrifying archaea. In contrast to other habitats that displayed constant diversification rates, marine planktonic AOA interestingly exhibit a very recent and accelerating diversification rate congruent with the lowest phylogenetic diversity observed in their habitats. This result suggested the existence of AOA communities with different evolutionary history in the different habitats.Conclusion and significanceBased on an up-to-date amoA phylogeny, this analysis provided insights into the possible evolutionary mechanisms and environmental parameters that shape AOA community assembly at global scale.

Dataset Information

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

Publications

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

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