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Rapid nitrification involving comammox and canonical Nitrospira at extreme pH in saline-alkaline lakes.

ABSTRACT: Nitrite-oxidizing bacteria (NOB) catalyse the second nitrification step and are the main biological source of nitrate. The most diverse and widespread NOB genus is Nitrospira, which also contains complete ammonia oxidizers (comammox) that oxidize ammonia to nitrate. To date, little is known about the occurrence and biology of comammox and canonical nitrite oxidizing Nitrospira in extremely alkaline environments. Here, we studied the seasonal distribution and diversity, and the effect of short-term pH changes on comammox and canonical Nitrospira in sediments of two saline, highly alkaline lakes. We identified diverse canonical and comammox Nitrospira clade A-like phylotypes as the only detectable NOB during more than a year, suggesting their major importance for nitrification in these habitats. Gross nitrification rates measured in microcosm incubations were highest at pH 10 and considerably faster than reported for other natural, aquatic environments. Nitrification could be attributed to canonical and comammox Nitrospira and to Nitrososphaerales ammonia-oxidizing archaea. Furthermore, our data suggested that comammox Nitrospira contributed to ammonia oxidation at an extremely alkaline pH of 11. These results identify saline, highly alkaline lake sediments as environments of uniquely strong nitrification with novel comammox Nitrospira as key microbial players.

SUBMITTER: Daebeler A

PROVIDER: S-EPMC10947350 | biostudies-literature | 2023 May

REPOSITORIES: biostudies-literature

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Rapid nitrification involving comammox and canonical Nitrospira at extreme pH in saline-alkaline lakes.

Daebeler Anne A Güell-Bujons Queralt Q Mooshammer Maria M Zechmeister Thomas T Herbold Craig W CW Richter Andreas A Wagner Michael M Daims Holger H

Environmental microbiology 20230203 5

Nitrite-oxidizing bacteria (NOB) catalyse the second nitrification step and are the main biological source of nitrate. The most diverse and widespread NOB genus is Nitrospira, which also contains complete ammonia oxidizers (comammox) that oxidize ammonia to nitrate. To date, little is known about the occurrence and biology of comammox and canonical nitrite oxidizing Nitrospira in extremely alkaline environments. Here, we studied the seasonal distribution and diversity, and the effect of short-te ...[more]

PMID: 36651641

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Project description:BackgroundThe discovery of microorganisms capable of complete ammonia oxidation to nitrate (comammox) has prompted a paradigm shift in our understanding of nitrification, an essential process in N cycling, hitherto considered to require both ammonia oxidizing and nitrite oxidizing microorganisms. This intriguing metabolism is unique to the genus Nitrospira, a diverse taxon previously known to only contain canonical nitrite oxidizers. Comammox Nitrospira have been detected in diverse environments; however, a global view of the distribution, abundance, and diversity of Nitrospira species is still incomplete.ResultsIn this study, we retrieved 55 metagenome-assembled Nitrospira genomes (MAGs) from newly obtained and publicly available metagenomes. Combined with publicly available MAGs, this constitutes the largest Nitrospira genome database to date with 205 MAGs, representing 132 putative species, most without cultivated representatives. Mapping of metagenomic sequencing reads from various environments against this database enabled an analysis of the distribution and habitat preferences of Nitrospira species. Comammox Nitrospira's ecological success is evident as they outnumber and present higher species-level richness than canonical Nitrospira in all environments examined, except for marine and wastewaters samples. The type of environment governs Nitrospira species distribution, without large-scale biogeographical signal. We found that closely related Nitrospira species tend to occupy the same habitats, and that this phylogenetic signal in habitat preference is stronger for canonical Nitrospira species. Comammox Nitrospira eco-evolutionary history is more complex, with subclades achieving rapid niche divergence via horizontal transfer of genes, including the gene encoding hydroxylamine oxidoreductase, a key enzyme in nitrification.ConclusionsOur study expands the genomic inventory of the Nitrospira genus, exposes the ecological success of complete ammonia oxidizers within a wide range of habitats, identifies the habitat preferences of (sub)lineages of canonical and comammox Nitrospira species, and proposes that horizontal transfer of genes involved in nitrification is linked to niche separation within a sublineage of comammox Nitrospira. Video Abstract.

Project description:The newly discovered complete ammonia-oxidizing (comammox) Nitrospira has been identified in different environments, including coastal environments, where salinity is one of the most important factors for the abundance and activity of nitrifiers. Here, we demonstrate the effect of salinity on comammox Nitrospira, canonical ammonia-oxidizing bacteria (AOB), and ammonia-oxidizing archaea (AOA) in the intertidal sediments of the Yangtze River estuary based on microcosm experiments, DNA stable-isotope probing (DNA-SIP), and potential ammonium-oxidation rate (PAR) tests for different groups of ammonia oxidizers with selective inhibitors. During microcosm incubations, the abundance of comammox Nitrospira was more sensitive to increased salinity than that of other ammonia oxidizers. The results obtained with DNA-SIP heavy fractions showed that the dominant phylotype in clade A.2 (containing genes involved in the adaptation to haloalkaline environments) had high proportions in comammox Nitrospira community under both freshwater (0.06% salinity) and highly saline water (3% salinity) conditions. In contrast, another phylotype of clade A.2 (which lacks these genes) was dominant only under freshwater conditions. The PARs confirmed that comammox Nitrospira presented greater contributions to nitrification under freshwater conditions with a PAR of 4.37 ± 0.53 mg N·day-1·kg soil-1 (54%) than under saline water conditions with a PAR of 0.60 ± 0.94 mg N·day-1·kg soil-1 (18%). Moreover, AOA were specific to saline water conditions, whereas AOB were common under both freshwater and saline water conditions (44% and 52%, respectively). The present study provided evidence that salinity markedly affects the activity of comammox Nitrospira, and that the salt sensitivity of different phylotypes varies. IMPORTANCE Complete ammonia oxidation (comammox) is a newly discovered type of nitrification through which ammonia is oxidized to nitrate in an organism. Comammox Nitrospira were abundantly found in coastal ecosystems and demonstrated high community diversity. Changes in salinity are considered one of the most important factors to comammox Nitrospira in coastal ecosystems; however, reports on the correlation between them remain inconsistent. Therefore, it is critical to experimentally determine the influence of salinity on comammox Nitrospira in the coastal ecosystem. This study demonstrated a clear effect of salinity on the abundance, activity, and relative contribution of different ammonia oxidizers, especially for comammox Nitrospira. To the best of our knowledge, this is the first study demonstrating comammox Nitrospira activity at seawater salinities, implying the existence of a salt-tolerant type comammox Nitrospira, despite its activity being much lower than in freshwater conditions. The indicated correlation between the activity of specific comammox Nitrospira and salinity is anticipated to provide insights into the distribution of comammox Nitrospira and their potential contributions in estuaries and coastal ecosystems.

Project description:Microbes commonly exist in diverse and complex communities where species interact, and their genomic repertoires evolve over time. Our understanding of species interaction and evolution has increased during the last decades, but most studies of evolutionary dynamics are based on single species in isolation or in experimental systems composed of few interacting species. Here, we use the microbial ecosystem found in groundwater-fed sand filter as a model to avoid this limitation. In these open systems, diverse microbial communities experience relatively stable conditions, and the coupling between chemical and biological processes is generally well defined. Metagenomic analysis of 12 sand filters communities revealed systematic co-occurrence of at least five comammox Nitrospira species, likely promoted by low ammonium concentrations. These Nitrospira species showed intrapopulation sequence diversity, although possible clonal expansion was detected in a few abundant local comammox populations. Nitrospira species showed low homologous recombination and strong purifying selection, the latter process being especially strong in genes essential in energy metabolism. Positive selection was detected for genes related to resistance to foreign DNA and phages. We found that, compared to other habitats, groundwater-fed sand filters impose strong purifying selection and low recombination on comammox Nitrospira populations. These results suggest that evolutionary processes are more affected by habitat type than by species identity. Together, this study improves our understanding of species interaction and evolution in complex microbial communities and sheds light on the environmental dependency of evolutionary processes. IMPORTANCE Microbial species interact with each other and their environment (ecological processes) and undergo changes in their genomic repertoire over time (evolutionary processes). How these two classes of processes interact is largely unknown, especially for complex communities, as most studies of microbial evolutionary dynamics consider single species in isolation or a few interacting species in simplified experimental systems. In this study, these limitations are circumvented by examining the microbial communities found in stable and well-described groundwater-fed sand filters. Combining metagenomics and strain-level analyses, we identified the microbial interactions and evolutionary processes affecting comammox Nitrospira, a recently discovered bacterial type capable of performing the whole nitrification process. We found that abundant and co-occurrent Nitrospira populations in groundwater-fed sand filters are characterized by low recombination and strong purifying selection. In addition, by comparing these observations with those obtained from Nitrospira species inhabiting other environments, we revealed that evolutionary processes are more affected by habitat type than by species identity.

Dataset Information

Rapid nitrification involving comammox and canonical Nitrospira at extreme pH in saline-alkaline lakes.

Publications

Rapid nitrification involving comammox and canonical Nitrospira at extreme pH in saline-alkaline lakes.

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