Global ecological pattern of ammonia-oxidizing archaea.

Huiluo Cao,Ji-Dong Gu,Jean-Christophe Auguet,Stefan Bertilsson

doi:10.1371/journal.pone.0052853

Abstract

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.

Highlights

For the cycling of nitrogen on earth, a number of critical processes carried out by microorganisms have been recognized, including dinitrogen (N2) fixation, ammonification, nitrification, denitrification, and anammox [1,2]
Our analysis considered all natural habitats, a special emphasis on amoA sequences originating from estuarine and freshwater systems was made and this is different from two previous studies on comparison between ammonia-oxidizing archaea (AOA) and ammonia-oxidizing bacteria (AOB) and aquatic habitats of AOA
Freshwater habitats have recently been proposed as one of the largest reservoirs of archaeal genetic diversity up to date [20,26], only a few freshwater planktonic habitats have been surveyed for amoA gene diversity. These include rivers [25], oligotrophic lakes [24,27], groundwater [28] and drinking water [29]. These studies on freshwater environments provided some new archaeal ammonia oxidizer lineages [24,25,27], indicating that planktonic freshwater habitats harbor typical amoA-containing ecotypes different from those found in soils and oceans [24]

Summary

Introduction

For the cycling of nitrogen on earth, a number of critical processes carried out by microorganisms have been recognized, including dinitrogen (N2) fixation, ammonification, nitrification, denitrification, and anammox (anaerobic ammonium oxidation) [1,2]. 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.

Results

Conclusion