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Acidification Enhances Hybrid N₂O Production Associated with Aquatic Ammonia-Oxidizing Microorganisms.

ABSTRACT: Ammonia-oxidizing microorganisms are an important source of the greenhouse gas nitrous oxide (N₂O) in aquatic environments. Identifying the impact of pH on N₂O production by ammonia oxidizers is key to understanding how aquatic greenhouse gas fluxes will respond to naturally occurring pH changes, as well as acidification driven by anthropogenic CO₂. We assessed N₂O production rates and formation mechanisms by communities of ammonia-oxidizing bacteria (AOB) and archaea (AOA) in a lake and a marine environment, using incubation-based nitrogen (N) stable isotope tracer methods with ¹⁵N-labeled ammonium (¹⁵[Formula: see text]) and nitrite (¹⁵[Formula: see text]), and also measurements of the natural abundance N and O isotopic composition of dissolved N₂O. N₂O production during incubations of water from the shallow hypolimnion of Lake Lugano (Switzerland) was significantly higher when the pH was reduced from 7.54 (untreated pH) to 7.20 (reduced pH), while ammonia oxidation rates were similar between treatments. In all incubations, added [Formula: see text] was the source of most of the N incorporated into N₂O, suggesting that the main N₂O production pathway involved hydroxylamine (NH₂OH) and/or [Formula: see text] produced by ammonia oxidation during the incubation period. A small but significant amount of N derived from exogenous/added ¹⁵[Formula: see text] was also incorporated into N₂O, but only during the reduced-pH incubations. Mass spectra of this N₂O revealed that [Formula: see text] and ¹⁵[Formula: see text] each contributed N equally to N₂O by a "hybrid-N₂O" mechanism consistent with a reaction between NH₂OH and [Formula: see text], or compounds derived from these two molecules. Nitrifier denitrification was not an important source of N₂O. Isotopomeric N₂O analyses in Lake Lugano were consistent with incubation results, as ¹⁵N enrichment of the internal N vs. external N atoms produced site preferences (25.0-34.4‰) consistent with NH₂OH-dependent hybrid-N₂O production. Hybrid-N₂O formation was also observed during incubations of seawater from coastal Namibia with ¹⁵[Formula: see text] and [Formula: see text]. However, the site preference of dissolved N₂O here was low (4.9‰), indicating that another mechanism, not captured during the incubations, was important. Multiplex sequencing of 16S rRNA revealed distinct ammonia oxidizer communities: AOB dominated numerically in Lake Lugano, and AOA dominated in the seawater. Potential for hybrid N₂O formation exists among both communities, and at least in AOB-dominated environments, acidification may accelerate this mechanism.

SUBMITTER: Frame CH

PROVIDER: S-EPMC5220105 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Increasing atmospheric CO2 concentrations are causing decreased pH over vast expanses of the ocean. This decreasing pH may alter biogeochemical cycling of carbon and nitrogen via the microbial process of nitrification, a key process that couples these cycles in the ocean, but which is often sensitive to acidic conditions. Recent reports indicate a decrease in oceanic nitrification rates under experimentally lowered pH. How composition and abundance of ammonia oxidizing bacteria (AOB) and archaea (AOA) assemblages respond to decreasing oceanic pH, however, is unknown. We sampled microbes from two different acidification experiments and used a combination of qPCR and functional gene microarrays for the ammonia monooxygenase gene (amoA) to assess how acidification alters the structure of ammonia oxidizer assemblages. We show that despite widely different experimental conditions, acidification consistently altered the community composition of AOB by increasing the relative abundance of taxa related to the Nitrosomonas ureae clade. In one experiment this increase was sufficient to cause an increase in the overall abundance of AOB. There were no systematic shifts in the community structure or abundance of AOA in either experiment. These different responses to acidification underscore the important role of microbial community structure in the resiliency of marine ecosystems. amoA gene diversity from two ocean acidification experiments, Monterey Bay experiment (two time points, ambient and acidified) and Vineyard Sound experiment (ambient and acifidied, with and without nutrients) examined with 2 two-color arrays (Cy3 and Cy5): the universal standard 20-mer oligo is printed to the slide with a 70-mer oligo (an archetype). Environmental DNA sequences (fluoresced with Cy3) within 15% of the 70-mer conjugated to a 20-mer oligo (fluoresced with Cy5) complementary to the universal standard will bind to the oligo probes on the array. Signal is the ratio of Cy3 to Cy5.

Project description:Microbial inhibition by high ammonia concentrations is a recurring problem that significantly restricts methane formation from intermediate acids, i.e., propionate and acetate, during anaerobic digestion of protein-rich waste material. Studying the syntrophic communities that perform acid conversion is challenging, due to their relatively low abundance within the microbial communities typically found in biogas processes and disruption of their cooperative behavior in pure cultures. To overcome these limitations, this study examined growth parameters and microbial community dynamics of highly enriched mesophilic and ammonia-tolerant syntrophic propionate and acetate-oxidizing communities and analyzed their metabolic activity and cooperative behavior using metagenomic and metatranscriptomic approaches. Cultivation in batch set-up demonstrated biphasic utilization of propionate, wherein acetate accumulated and underwent oxidation before complete degradation of propionate. Three key species for syntrophic acid degradation were inferred from genomic sequence information and gene expression: a syntrophic propionate-oxidizing bacterium (SPOB) "Candidatus Syntrophopropionicum ammoniitolerans", a syntrophic acetate-oxidizing bacterium (SAOB) Syntrophaceticus schinkii and a novel hydrogenotrophic methanogen, for which we propose the provisional name "Candidatus Methanoculleus ammoniitolerans". The results revealed consistent transcriptional profiles of the SAOB and the methanogen both during propionate and acetate oxidation, regardless of the presence of an active propionate oxidizer. Gene expression indicated versatile capabilities of the two syntrophic bacteria, utilizing both molecular hydrogen and formate as an outlet for reducing equivalents formed during acid oxidation, while conserving energy through build-up of sodium/proton motive force. The methanogen used hydrogen and formate as electron sources. Furthermore, results of the present study provided a framework for future research into ammonia tolerance, mobility, aggregate formation and interspecies cooperation.

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Acidification Enhances Hybrid N₂O Production Associated with Aquatic Ammonia-Oxidizing Microorganisms.

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Acidification Enhances Hybrid N₂O Production Associated with Aquatic Ammonia-Oxidizing Microorganisms.