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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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Related in: MedlinePlus

Diversification rates plotted as lineage through-time (ltt) plots based on ultrametric trees (penalized likelihood method).Bar plot in the upper left corner indicates the values γ (i.e. rate of cladogenesis) for each habitat.
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pone-0052853-g004: Diversification rates plotted as lineage through-time (ltt) plots based on ultrametric trees (penalized likelihood method).Bar plot in the upper left corner indicates the values γ (i.e. rate of cladogenesis) for each habitat.

Mentions: The marked differences in AOA phylogenetic diversity and community structure among different habitats raised the question of the evolutionary processes underlying these patterns. One apparent reason may be the existence of distinct rates of cladogenesis over time among habitats. As phylogenies derived from molecular data, phylogenetic trees provide an indirect record of speciation events [52], the amoA phylogeny inferred in this study can be used to test this hypothesis. Accumulation of lineages as a function of a relative scale of time (ltt plot) were plotted for each habitat in order to assess departure from a constant rate of cladogenesis (i.e. γ = 0). Except for the marine water column, very similar ltt plots were observed for all habitats with a constant accumulation of lineages initiated closer to the root than to the tips of the tree were observed (Fig. 4). This resulted in constant diversification rates for the estuarine sediment and freshwater habitats and decelerating rates for the remaining habitats. These results must be taken cautiously as microbial evolutionary inferences suffer from limitations such as the lack of fossil records and the unknown range of microbial diversity [53]. The latter aspect is critical since the gamma statistical value calculated with the method developed by Pybus and Harvey [54] results in increasingly negative gamma values as the fraction of the sampled diversity decreases [55]. Hence, it is possible that the negative gamma values obtained would follow the general pattern for microorganisms assuming a constant diversification rate [55] if an exhaustive sampling of amoA diversity could be made. Departure from this general constant diversification pattern (i.e. acceleration or deceleration) has been observed previously in bacteria [56], archaea [57] and denitrifiers [21]. Very recently, it has been shown that the whole AOA community exhibited two fast diversification events separated by a long steady-state episode [22]. Interestingly, in the present study, only one habitat, the marine water column habitat, differed significantly from the general constant diversification pattern and displayed a recent diversification marked by an increase in the rate of cladogenesis (i.e. γ = 7.2±5.1) toward present time (Fig. 4). Discrepancies in the rate of cladogenesis and diversification patterns between both studies may rely in the methods used to calculate them. Here, we used a maximum likelihood method assuming a molecular clock since it provides a more reliable estimate of diversification than non-molecular clock methods [55]. The recent diversification of marine planktonic amoA sequences is consistent with the low PD and PSV values observed for this habitat. The factors resulting in an acceleration of the cladogenesis rate cannot be identified in this work but they may lie in the ecological context of speciation and extinction within marine planktonic systems.


Global ecological pattern of ammonia-oxidizing archaea.

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

Diversification rates plotted as lineage through-time (ltt) plots based on ultrametric trees (penalized likelihood method).Bar plot in the upper left corner indicates the values γ (i.e. rate of cladogenesis) for each habitat.
© Copyright Policy
Related In: Results  -  Collection

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

pone-0052853-g004: Diversification rates plotted as lineage through-time (ltt) plots based on ultrametric trees (penalized likelihood method).Bar plot in the upper left corner indicates the values γ (i.e. rate of cladogenesis) for each habitat.
Mentions: The marked differences in AOA phylogenetic diversity and community structure among different habitats raised the question of the evolutionary processes underlying these patterns. One apparent reason may be the existence of distinct rates of cladogenesis over time among habitats. As phylogenies derived from molecular data, phylogenetic trees provide an indirect record of speciation events [52], the amoA phylogeny inferred in this study can be used to test this hypothesis. Accumulation of lineages as a function of a relative scale of time (ltt plot) were plotted for each habitat in order to assess departure from a constant rate of cladogenesis (i.e. γ = 0). Except for the marine water column, very similar ltt plots were observed for all habitats with a constant accumulation of lineages initiated closer to the root than to the tips of the tree were observed (Fig. 4). This resulted in constant diversification rates for the estuarine sediment and freshwater habitats and decelerating rates for the remaining habitats. These results must be taken cautiously as microbial evolutionary inferences suffer from limitations such as the lack of fossil records and the unknown range of microbial diversity [53]. The latter aspect is critical since the gamma statistical value calculated with the method developed by Pybus and Harvey [54] results in increasingly negative gamma values as the fraction of the sampled diversity decreases [55]. Hence, it is possible that the negative gamma values obtained would follow the general pattern for microorganisms assuming a constant diversification rate [55] if an exhaustive sampling of amoA diversity could be made. Departure from this general constant diversification pattern (i.e. acceleration or deceleration) has been observed previously in bacteria [56], archaea [57] and denitrifiers [21]. Very recently, it has been shown that the whole AOA community exhibited two fast diversification events separated by a long steady-state episode [22]. Interestingly, in the present study, only one habitat, the marine water column habitat, differed significantly from the general constant diversification pattern and displayed a recent diversification marked by an increase in the rate of cladogenesis (i.e. γ = 7.2±5.1) toward present time (Fig. 4). Discrepancies in the rate of cladogenesis and diversification patterns between both studies may rely in the methods used to calculate them. Here, we used a maximum likelihood method assuming a molecular clock since it provides a more reliable estimate of diversification than non-molecular clock methods [55]. The recent diversification of marine planktonic amoA sequences is consistent with the low PD and PSV values observed for this habitat. The factors resulting in an acceleration of the cladogenesis rate cannot be identified in this work but they may lie in the ecological context of speciation and extinction within marine planktonic systems.

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