Acidification alters the composition of ammonia‑oxidizing microbial assemblages in marine mesocosms

Bowen, Jennifer L.; Kearns, Patrick J.; Holcomb, Michael; Ward, Bess B.

doi:10.3354/meps10526

Cited by 19 publications

(18 citation statements)

References 36 publications

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“…Our results are not necessarily predictive of the long-term influence of acidification on N 2 O production by ammonia oxidizers, since acidification may also change ammonia oxidizer community composition (Bowen et al, 2013) and pH decreases may have cascading chemical and biological effects in lake and ocean ecosystems. However, our results are applicable to environments that experience rapid changes in pH such as stratified lakes that undergo episodic mixing or rapid influx of acidified precipitation, and ocean upwelling zones where CO 2 -rich, low-pH deeper water may enhance N 2 O production when it comes in contact with shallower ammonia-oxidizing communities.…”

Section: Discussionmentioning

confidence: 76%

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

et al. 2017

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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 (15NH4+) and nitrite (15NO2−), 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 NH4+ was the source of most of the N incorporated into N2O, suggesting that the main N2O production pathway involved hydroxylamine (NH2OH) and/or NO2− produced by ammonia oxidation during the incubation period. A small but significant amount of N derived from exogenous/added 15NO2− was also incorporated into N2O, but only during the reduced-pH incubations. Mass spectra of this N2O revealed that NH4+ and 15NO2− each contributed N equally to N2O by a “hybrid-N2O” mechanism consistent with a reaction between NH2OH and NO2−, 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 15NH4+ and NO2−. 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.

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Section: Discussionmentioning

confidence: 76%

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

et al. 2017

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“…AOA and AOB may adjust their metabolism and physiology to alternative pathways that are not connected to amoA and amoB enzymes. No systematic shift in AOA and AOB abundance was found in coastal marine communities during an acidification experiment, but a consistent relative increase in abundance of a AOB taxa related to the Nitrosomonas ureae clade was apparent (Bowen et al, 2013). A change in expression of a specific set of ammonia transporters in AOAs may alter the affinity for ammonium, potentially facilitating functional heterogeneity (Offre, Kerou, Spang, & Schleper, 2014).…”

Section: Nitrificationmentioning

confidence: 94%

“…There is a discrepancy in the response to OA of ammonium oxidation rates (negative) and the corresponding AOA and AOB gene abundance (nonsignificant positive; Supporting information Table S2). This may reflect the low number of gene abundance studies (Laverock et al, 2013;Tait, Laverock, & Widdicombe, 2014) and also disparities between amoA gene abundance, transcripts, and associated enzyme activity (Bowen, Kearns, Holcomb, & Ward, 2013;Glanemann, Loos, Gorret, Willis, & O´Brien X, Lessard P, Sinskey A, 2003;Hatzenpichler, 2012;Rocca et al, 2015). AOA and AOB may adjust their metabolism and physiology to alternative pathways that are not connected to amoA and amoB enzymes.…”

Section: Nitrificationmentioning

confidence: 99%

The response of the marine nitrogen cycle to ocean acidification

Wannicke

Frey

Law

et al. 2018

Global Change Biology

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Ocean acidification (OA), arising from the influx of anthropogenically generated carbon, poses a massive threat to the ocean ecosystems. Our knowledge of the effects of elevated anthropogenic CO in marine waters and its effect on the performance of single species, trophic interactions, and ecosystems is increasing rapidly. However, our understanding of the biogeochemical cycling of nutrients such as nitrogen is less advanced and lacks a comprehensive overview of how these processes may change under OA. We conducted a systematic review and meta-analysis of eight major nitrogen transformation processes incorporating 49 publications to synthesize current scientific understanding of the effect of OA on nitrogen cycling in the future ocean by 2100. The following points were identified by our meta-analysis: (a) Diazotrophic nitrogen fixation is likely enhanced by 29% ± 4% under OA; (b) species- and strain-specific responses of nitrogen fixers to OA were detectable, which may result in alterations in microbial community composition in the future ocean; (c) nitrification processes were reduced by a factor of 29% ± 10%; (d) declines in nitrification rates were not reflected by nitrifier abundance; and (e) contrasting results in unispecific culture experiments versus natural communities were apparent for nitrogen fixation and denitrification. The net effect of the nitrogen cycle process responses also suggests there may be a shift in the relative nitrogen pools, with excess ammonium originating from CO -fertilized diazotrophs. This regenerated inorganic nitrogen may recycle in the upper water column increasing the relative importance of the ammonium-fueled regenerated production. However, several feedback mechanisms with other chemical cycles, such as oxygen, and interaction with other climate change stressors may counteract these findings. Finally, our review highlights the shortcomings and gaps in current understanding of the potential changes in nitrogen cycling under future climate and emphasizes the need for further ecosystem studies.

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“…Bowen et al reported that microbial groups capable of ammonia oxidization have different responses to acidification. Some ammonia oxidization bacteria are significantly influenced by ocean acidification, but not AOA (Bowen et al, ). A similar result was also reported by Tait et al () who found that ammonia oxidizing bacteria and archaea in marine sediments have different pH optima.…”

Section: Discussionmentioning

confidence: 99%

Ocean Acidification Regulates the Activity, Community Structure, and Functional Potential of Heterotrophic Bacterioplankton in an Oligotrophic Gyre

et al. 2019

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Ocean acidification (OA), a consequence of increased global carbon dioxide (CO 2 ) emissions, is considered a major threat to marine ecosystems. Its effects on bacterioplankton activity, diversity, and community composition have received considerable attention. However, the direct impact of OA on heterotrophic bacterioplankton is often masked by the significant response of phytoplankton due to the close coupling of heterotrophic bacterioplankton and autotrophs. Here we investigated the responses of a heterotrophic bacterioplankton assemblage to high pCO 2 (790-ppm) treatment in warm tropical western Pacific waters by conducting a microcosm experiment in dark for 12 days. Heterotrophic bacterioplankton abundance and production were enhanced by OA over the first 6 days of incubation, while the diversity and species richness were negatively affected. Bacterioplankton community composition in the high pCO 2 treatment changed faster than that in the control. The molecular ecological network analysis showed that the elevated CO 2 changed the overall connections among the bacterial community and resulted in a simple network under high CO 2 condition. Species-specific responses to OA were observed and could be attributed to the different life strategies and to the ability of a given species to adapt to environmental conditions. In addition, high-throughput functional gene array analysis revealed that genes related to carbon and nitrogen cycling were positively affected by acidification. Together, our findings suggest that OA has direct effects on heterotrophic bacterioplankton in a low-latitude warm ocean and may therefore affect global biogeochemical cycles.

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Acidification alters the composition of ammonia‑oxidizing microbial assemblages in marine mesocosms

Cited by 19 publications

References 36 publications

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

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

The response of the marine nitrogen cycle to ocean acidification

Ocean Acidification Regulates the Activity, Community Structure, and Functional Potential of Heterotrophic Bacterioplankton in an Oligotrophic Gyre

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