Ecological dynamics explain modular denitrification in the ocean

Microorganisms in marine oxygen minimum zones (OMZs) drive globally impactful biogeochemical processes. One such process is multistep denitrification (NO<sub>3</sub><sup>-</sup>→NO<sub>2</sub><sup>-</sup>→NO→N<sub>2</sub>O→N<sub>2</sub>), which dominates OMZ bioavailable nitrogen (N) loss and nitrous oxide (N<sub>2</sub>O) production. Denitrification-derived N loss is typically measured and modeled as a single step, but observations reveal that most denitrifiers in OMZs contain subsets ("modules") of the complete pathway. Here, we identify the ecological mechanisms sustaining diverse denitrifiers, explain the prevalence of certain modules, and examine the implications for N loss. We describe microbial functional types carrying out diverse denitrification modules by their underlying redox chemistry, constraining their traits with thermodynamics and pathway length penalties, in an idealized OMZ ecosystem model. Biomass yields of single-step modules increase along the denitrification pathway when organic matter (OM) limits growth, which explains the viability of populations respiring NO<sub>2</sub><sup>-</sup> and N<sub>2</sub>O in a NO<sub>3</sub><sup>-</sup>-filled ocean. Results predict denitrifier community succession along environmental gradients: Pathway length increases as the limiting substrate shifts from OM to N, suggesting a niche for the short NO<sub>3</sub><sup>-</sup>→NO<sub>2</sub><sup>-</sup> module in free-living, OM-limited communities, and for the complete pathway in organic particle-associated communities, consistent with observations. The model captures and mechanistically explains the observed dominance and higher oxygen tolerance of the NO<sub>3</sub><sup>-</sup>→NO<sub>2</sub><sup>-</sup> module. Results also capture observations that NO<sub>3</sub><sup>-</sup> is the dominant source of N<sub>2</sub>O. Our framework advances the mechanistic understanding of the relationship between microbial ecology and N loss in the ocean and can be extended to other processes and environments.

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Publication Details

Journal
Proceedings of the National Academy of Sciences
Published
2024-12-18
DOI
https://doi.org/10.1073/pnas.2417421121
Citations
18
Primary Topic
Wastewater Treatment and Nitrogen Removal
Type
article
Field-Weighted Citation Impact
2.39

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article

Ecological dynamics explain modular denitrification in the ocean

Xin Sun, Emily J. Zakem, Pearse Buchanan, Irene H. Zhang et al.
18 citations
Proceedings of the National Academy of Sciences
Wastewater Treatment and Nitrogen Removal
2.39
article

Ecological dynamics explain modular denitrification in the ocean

Xin Sun, Emily J. Zakem, Pearse Buchanan, Irene H. Zhang, Magdalena San Román, Andrew R. Babbin
article en
18 citations

Abstract

Microorganisms in marine oxygen minimum zones (OMZs) drive globally impactful biogeochemical processes. One such process is multistep denitrification (NO<sub>3</sub><sup>-</sup>→NO<sub>2</sub><sup>-</sup>→NO→N<sub>2</sub>O→N<sub>2</sub>), which dominates OMZ bioavailable nitrogen (N) loss and nitrous oxide (N<sub>2</sub>O) production. Denitrification-derived N loss is typically measured and modeled as a single step, but observations reveal that most denitrifiers in OMZs contain subsets ("modules") of the complete pathway. Here, we identify the ecological mechanisms sustaining diverse denitrifiers, explain the prevalence of certain modules, and examine the implications for N loss. We describe microbial functional types carrying out diverse denitrification modules by their underlying redox chemistry, constraining their traits with thermodynamics and pathway length penalties, in an idealized OMZ ecosystem model. Biomass yields of single-step modules increase along the denitrification pathway when organic matter (OM) limits growth, which explains the viability of populations respiring NO<sub>2</sub><sup>-</sup> and N<sub>2</sub>O in a NO<sub>3</sub><sup>-</sup>-filled ocean. Results predict denitrifier community succession along environmental gradients: Pathway length increases as the limiting substrate shifts from OM to N, suggesting a niche for the short NO<sub>3</sub><sup>-</sup>→NO<sub>2</sub><sup>-</sup> module in free-living, OM-limited communities, and for the complete pathway in organic particle-associated communities, consistent with observations. The model captures and mechanistically explains the observed dominance and higher oxygen tolerance of the NO<sub>3</sub><sup>-</sup>→NO<sub>2</sub><sup>-</sup> module. Results also capture observations that NO<sub>3</sub><sup>-</sup> is the dominant source of N<sub>2</sub>O. Our framework advances the mechanistic understanding of the relationship between microbial ecology and N loss in the ocean and can be extended to other processes and environments.

Proceedings of the National Academy of SciencesVol. 121(52)
University of Southern California (US), Consejo Superior de Investigaciones Científicas (ES), Universidad de Salamanca (ES), Carnegie Institution for Science (US), Health Sciences and Nutrition (AU), Seth Research Foundation (IN), Instituto de Biología Funcional y Genómica (ES), Massachusetts Institute of Technology (US)
National Science Foundation, Simons Foundation, Carnegie Institution for Science
Life below water
Openalex Percentile: Top 11%
Wastewater Treatment and Nitrogen Removal
2.39
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