Global Ecological Pattern of Ammonia-Oxidizing Archaea

BACKGROUND: The 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 RESULTS: We 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 SIGNIFICANCE: Based 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.