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Global ecological pattern of ammonia-oxidizing archaea.

Cao H, Auguet JC, Gu JD - PLoS ONE (2013)

Bottom Line: 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.This result suggested the existence of AOA communities with different evolutionary history in the different habitats.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.

View Article: PubMed Central - PubMed

Affiliation: Laboratory of Environmental Microbiology and Toxicology, School of Biological Sciences, The University of Hong Kong, Hong Kong, China.

ABSTRACT

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.

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PCoA analyses for archaeal amoA gene assemblages based on the different environmental factors calculated by the online Fast UniFrac software (A, living style; B, oxygen; C, salinity; D, temperature).
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pone-0052853-g003: PCoA analyses for archaeal amoA gene assemblages based on the different environmental factors calculated by the online Fast UniFrac software (A, living style; B, oxygen; C, salinity; D, temperature).

Mentions: The 85 environmental AOA clone libraries analyzed in this study were sorted into a principal coordinate analysis (PCoA) plot according to phylogenetic community similarity (Fig. 2). In agreement with the concept of habitat filtering [38] and as observed in previous studies on ribosomal or functional genes [19]–[23], AOA communities were more similar within habitats than among habitats (R2 = 0.16, P = 0.001) (Fig. 2). Among the environmental variables common to all studies (i.e. salinity, lifestyle, temperature and oxygenation), salinity was the strongest factor explaining AOA community structure patterns. Salinity alone accounted for 8.6% (P = 0.003) of the total variance from the Unifrac analysis (Fig. 3a) and clearly separated saline habitats from non-saline habitats in a hierarchical clustering analysis (Fig. 2b). Previous studies analyzing prokaryotic phylogenies based on ribosomal [19], [20] and functional genes [23] have also revealed a clear separation between freshwater and marine lineages, suggesting that, similar to eukaryotes, salinity represented one of the most important evolutionary barrier preventing frequent environmental transitions [39]. Jones et al. [21] showed that this evolutionary segregation also applies to the nirS and nirK denitrifying genes. However, due to marked incongruences between ribosomal and denitrifying gene phylogenies, they could not rule out an important effect of horizontal gene transfer (HGT). Unlike denitrifying genes, archaeal amoA phylogeny seemed to be largely congruent with the archaeal ribosomal phylogeny [24], [40], [41]. Therefore, our analysis suggested that salinity rather than HGT may have a more significantly influence on the evolution of AOA and may be one of the most important evolutionary factors for N transforming microorganisms.


Global ecological pattern of ammonia-oxidizing archaea.

Cao H, Auguet JC, Gu JD - PLoS ONE (2013)

PCoA analyses for archaeal amoA gene assemblages based on the different environmental factors calculated by the online Fast UniFrac software (A, living style; B, oxygen; C, salinity; D, temperature).
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3585293&req=5

pone-0052853-g003: PCoA analyses for archaeal amoA gene assemblages based on the different environmental factors calculated by the online Fast UniFrac software (A, living style; B, oxygen; C, salinity; D, temperature).
Mentions: The 85 environmental AOA clone libraries analyzed in this study were sorted into a principal coordinate analysis (PCoA) plot according to phylogenetic community similarity (Fig. 2). In agreement with the concept of habitat filtering [38] and as observed in previous studies on ribosomal or functional genes [19]–[23], AOA communities were more similar within habitats than among habitats (R2 = 0.16, P = 0.001) (Fig. 2). Among the environmental variables common to all studies (i.e. salinity, lifestyle, temperature and oxygenation), salinity was the strongest factor explaining AOA community structure patterns. Salinity alone accounted for 8.6% (P = 0.003) of the total variance from the Unifrac analysis (Fig. 3a) and clearly separated saline habitats from non-saline habitats in a hierarchical clustering analysis (Fig. 2b). Previous studies analyzing prokaryotic phylogenies based on ribosomal [19], [20] and functional genes [23] have also revealed a clear separation between freshwater and marine lineages, suggesting that, similar to eukaryotes, salinity represented one of the most important evolutionary barrier preventing frequent environmental transitions [39]. Jones et al. [21] showed that this evolutionary segregation also applies to the nirS and nirK denitrifying genes. However, due to marked incongruences between ribosomal and denitrifying gene phylogenies, they could not rule out an important effect of horizontal gene transfer (HGT). Unlike denitrifying genes, archaeal amoA phylogeny seemed to be largely congruent with the archaeal ribosomal phylogeny [24], [40], [41]. Therefore, our analysis suggested that salinity rather than HGT may have a more significantly influence on the evolution of AOA and may be one of the most important evolutionary factors for N transforming microorganisms.

Bottom Line: 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.This result suggested the existence of AOA communities with different evolutionary history in the different habitats.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.

View Article: PubMed Central - PubMed

Affiliation: Laboratory of Environmental Microbiology and Toxicology, School of Biological Sciences, The University of Hong Kong, Hong Kong, China.

ABSTRACT

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.

Show MeSH
Related in: MedlinePlus