Abundant nitrite-oxidizing metalloenzymes in the mesopelagic zone of the tropical Pacific Ocean

Abstract

Numerous biogeochemical reactions occur within the oceans’ major oxygen minimum zones, but less attention has been paid to the open ocean extremities of these zones. Here we report measurements on oxygen minimum zone waters from the Eastern to the Central Tropical North Pacific, which we analysed using metaproteomic techniques to discern the microbial functions present and their influence on biogeochemical cycling. We found nitrite oxidoreductase—an iron-rich enzyme from Nitrospina bacteria—to be one of the most abundant microbial proteins present in the mesopelagic zone, with over 60 billion molecules per litre. Estimated reaction rates imply that this enzyme is undersaturated and that its high abundance provides a latent mesopelagic catalytic capacity to rapidly oxidize nitrite derived from episodic fluxes of degrading sinking organic matter. In addition, given the enzyme’s intensive iron demand, its high abundance represents a previously unrecognized microbial reservoir within suboxic mesopelagic zones. Nitrite oxidoreductase may also contribute to other reactions involving nitrogen and redox-sensitive metals. We suggest that the abundance and extent of nitrite oxidoreductase may increase with continued deoxygenation in the oceans, and result in increased mesopelagic demand for iron and other potential changes to marine biogeochemical cycles.

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Fig. 1: Station locations, hydrographic features and Nxr distributions for the Metzyme and ProteOMZ expeditions.
Fig. 2: Abundant Nxr in the Central Pacific Ocean and in a Nitrospira culture.
Fig. 3: Targeted metaproteomic analyses of peptides from Nxr at Metzyme station 3.
Fig. 4: Nxr enzyme concentrations, iron use and estimated reaction rates based on targeted metaproteomic analyses.
Fig. 5: Nxr, oxygen and nitrous oxide in the Central Pacific OMZ.

Data availability

Environmental data and processed global and targeted metaproteomic results from Metzyme and ProteOMZ expeditions are available at https://www.bco-dmo.org/ under projects 2236 and 685696 and dataset 806510, and the global metaproteomes can be explored through the Ocean Protein Portal (https://www.oceanproteinportal.org). The metagenomic assembly used for peptide-to-spectrum matching is available at NCBI under accession GCA_900411625. Targeted Nxr concentrations and NOB abundances are available within Supplementary Tables 9 and 8. Raw mass spectra are available in PRIDE and ProteomeXchange as project number PXD009712.

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Acknowledgements

We thank the captain and crews of the RV Kilo Moana and RV Falkor for their assistance. We appreciate the sampling assistance from T. Goepfert, N. Held, N. Hawco, T. Horner, C. Hau, and D. Wang. Metagenome and N. marina sequencing was provided by the Department of Energy Joint Genome Institute. Time aboard the RV Falkor was provided by the Schmidt Ocean Institute. Funding for this research in the Saito laboratory was provided by the Gordon and Betty Moore Foundation (3782) and the National Science Foundation (OCE-1031271, 1736599, 1657766, 1850719, 1924554). J.K.S. was supported by the NASA Postdoctoral Fellowship Program. A.E.S. was supported by the Sloan Foundation, the Simons Foundation and United States National Science Foundation award OCE-1437310. A portion of this research used resources at the DOE Joint Genome Institute sponsored by the Office of Biological and Environmental Research and operated under contract DE-AC02-05CH11231 (JGI). C.L.D. and D.K. were supported by NSF grant OCE-1259994.

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Contributions

M.A.S. led field expeditions, collected samples, analysed datasets and wrote the manuscript. M.R.M. analysed samples by mass spectrometry and developed targeted proteomic assays. D.M.M. collected and extracted metaproteomic samples. A.E.S. participated in the expeditions, contributed to interpretations, measured NOB abundances, cultured Nb-295 and edited the manuscript. C.L.D. analysed metagenomics datasets, provided metagenomic assemblies and contributed to the manuscript. P.A.R. analysed 15N-NO3 samples and contributed to the manuscript discussion. J.K.S. contributed to metaproteomic informatic analyses and manuscript interpretations. D.K. contributed to metagenomic informatic analyses. M.W. contributed N2O and nitrite data from KM0405. C.H.L. co-led the Metzyme field expedition, collected samples and contributed to the manuscript discussions. J.B.W. and F.V. contributed to nitrifier culture experiments and manuscript discussions.

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Correspondence to Mak A. Saito.

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Supplementary Tables 1–9, Figs. 1–28 and references.

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Saito, M.A., McIlvin, M.R., Moran, D.M. et al. Abundant nitrite-oxidizing metalloenzymes in the mesopelagic zone of the tropical Pacific Ocean. Nat. Geosci. 13, 355–362 (2020). https://doi.org/10.1038/s41561-020-0565-6

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