Limits...
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.

Show MeSH

Related in: MedlinePlus

Phylogenetic tree based on archaeal amoA gene sequences from the variable samples on the global level using the maximum likelihood (ML) criterion.The credible support over 70% for each node was indicated with round circle on the node. The outer color circle around the phylogenetic tree suggested the different habitats.
© Copyright Policy
Related In: Results  -  Collection


getmorefigures.php?uid=PMC3585293&req=5

pone-0052853-g001: Phylogenetic tree based on archaeal amoA gene sequences from the variable samples on the global level using the maximum likelihood (ML) criterion.The credible support over 70% for each node was indicated with round circle on the node. The outer color circle around the phylogenetic tree suggested the different habitats.

Mentions: Our amoA gene phylogenetic tree 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 (Fig. 1) following the nomenclature of Pester et al. (2012). Unlike the latter phylogeny, the Nitrososphaera cluster was located at the base of the tree and was not a monophyletic sister cluster of the Nitrosocaldus and Nitrosopumilus/Nitrosotalea clusters. The discrepancies between both phylogenies may be explained by the fact that Pester's phylogeny is based on sequences available publically in 2010. Since then, a significant amount of new sequences have been made available in the public databases and particularly from low salinity or freshwater habitats like estuarine and freshwater systems [11], [24], [25]. Although 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]. Because these freshwater sequences were also clustered with those from acidic soils, e.g. the enrichment of Candidatus Nitrosotalea devanaterra, this cluster was named as Nitrosotalea cluster in agreement with Pester et al (Fig. 1) [30]. Freshwater sequences and those from low salinity environments, i.e. estuaries [31]–[33] and hot springs [8], [9], [34]–[37] formed another non-monophyletic group of several secondary clusters within the Nitrosopumilus cluster. This group of clusters, containing the low salinity archaeal Nitrosoarchaeum limnia, is separated clearly from other saline clusters and is temporally named as Low Salinity Environment Cluster (Fig. 1).


Global ecological pattern of ammonia-oxidizing archaea.

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

Phylogenetic tree based on archaeal amoA gene sequences from the variable samples on the global level using the maximum likelihood (ML) criterion.The credible support over 70% for each node was indicated with round circle on the node. The outer color circle around the phylogenetic tree suggested the different habitats.
© Copyright Policy
Related In: Results  -  Collection

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

pone-0052853-g001: Phylogenetic tree based on archaeal amoA gene sequences from the variable samples on the global level using the maximum likelihood (ML) criterion.The credible support over 70% for each node was indicated with round circle on the node. The outer color circle around the phylogenetic tree suggested the different habitats.
Mentions: Our amoA gene phylogenetic tree 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 (Fig. 1) following the nomenclature of Pester et al. (2012). Unlike the latter phylogeny, the Nitrososphaera cluster was located at the base of the tree and was not a monophyletic sister cluster of the Nitrosocaldus and Nitrosopumilus/Nitrosotalea clusters. The discrepancies between both phylogenies may be explained by the fact that Pester's phylogeny is based on sequences available publically in 2010. Since then, a significant amount of new sequences have been made available in the public databases and particularly from low salinity or freshwater habitats like estuarine and freshwater systems [11], [24], [25]. Although 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]. Because these freshwater sequences were also clustered with those from acidic soils, e.g. the enrichment of Candidatus Nitrosotalea devanaterra, this cluster was named as Nitrosotalea cluster in agreement with Pester et al (Fig. 1) [30]. Freshwater sequences and those from low salinity environments, i.e. estuaries [31]–[33] and hot springs [8], [9], [34]–[37] formed another non-monophyletic group of several secondary clusters within the Nitrosopumilus cluster. This group of clusters, containing the low salinity archaeal Nitrosoarchaeum limnia, is separated clearly from other saline clusters and is temporally named as Low Salinity Environment Cluster (Fig. 1).

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