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© The Author(s), 2022. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Saunders, J. K., McIlvin, M. R., Dupont, C. L., Kaul, D., Moran, D. M., Horner, T., Laperriere, S. M., Webb, E. A., Bosak, T., Santoro, A. E., & Saito, M. A. Microbial functional diversity across biogeochemical provinces in the central Pacific Ocean. Proceedings of the National Academy of Sciences of the United States of America, 119(37),(2022): e2200014119, https://doi.org/10.1073/pnas.2200014119., Enzymes catalyze key reactions within Earth’s life-sustaining biogeochemical cycles. Here, we use metaproteomics to examine the enzymatic capabilities of the microbial community (0.2 to 3 µm) along a 5,000-km-long, 1-km-deep transect in the central Pacific Ocean. Eighty-five percent of total protein abundance was of bacterial origin, with Archaea contributing 1.6%. Over 2,000 functional KEGG Ontology (KO) groups were identified, yet only 25 KO groups contributed over half of the protein abundance, simultaneously indicating abundant key functions and a long tail of diverse functions. Vertical attenuation of individual proteins displayed stratification of nutrient transport, carbon utilization, and environmental stress. The microbial community also varied along horizontal scales, shaped by environmental features specific to the oligotrophic North Pacific Subtropical Gyre, the oxygen-depleted Eastern Tropical North Pacific, and nutrient-rich equatorial upwelling. Some of the most abundant proteins were associated with nitrification and C1 metabolisms, with observed interactions between these pathways. The oxidoreductases nitrite oxidoreductase (NxrAB), nitrite reductase (NirK), ammonia monooxygenase (AmoABC), manganese oxidase (MnxG), formate dehydrogenase (FdoGH and FDH), and carbon monoxide dehydrogenase (CoxLM) displayed distributions indicative of biogeochemical status such as oxidative or nutritional stress, with the potential to be more sensitive than chemical sensors. Enzymes that mediate transformations of atmospheric gases like CO, CO2, NO, methanethiol, and methylamines were most abundant in the upwelling region. We identified hot spots of biochemical transformation in the central Pacific Ocean, highlighted previously understudied metabolic pathways in the environment, and provided rich empirical data for biogeochemical models critical for forecasting ecosystem response to climate change., Funding for this research was provided by the Gordon and Betty Moore Foundation (grants 3782 and 8453), the US NSF (NSF grants OCE-1924554, 2123055, 2125063, 2048774, and 2026933), the Center for Chemical Currencies on a Microbial Planet (NSF grant OCE-2019589), and the US NIH General Medicine (grant GM135709-01A1). J.K.S. was supported by a NASA Postdoctoral Program Fellowship with the NASA Astrobiology Program, administered by Universities Space Research Association under contract with NASA. A.E.S. was supported by the Sloan Foundation, the Simons Foundation, and NSF grant OCE-1437310. A portion of this research used resources at the US Department of Energy JGI 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 grants OCE-1558453 and OCE-2049299. T.H. was supported by NSF grant OCE-2023456.

Enzymes catalyze key reactions within Earth’s life-sustaining biogeochemical cycles. Here, we use metaproteomics to examine the enzymatic capabilities of the microbial community (0.2 to 3 µm) along a 5,000-km-long, 1-km-deep transect in the central Pacific Ocean. Eighty-five percent of total protein abundance was of bacterial origin, with Archaea contributing 1.6%. Over 2,000 functional KEGG Ontology (KO) groups were identified, yet only 25 KO groups contributed over half of the protein abundance, simultaneously indicating abundant key functions and a long tail of diverse functions. Vertical attenuation of individual proteins displayed stratification of nutrient transport, carbon utilization, and environmental stress. The microbial community also varied along horizontal scales, shaped by environmental features specific to the oligotrophic North Pacific Subtropical Gyre, the oxygen-depleted Eastern Tropical North Pacific, and nutrient-rich equatorial upwelling. Some of the most abundant proteins were associated with nitrification and C1 metabolisms, with observed interactions between these pathways. The oxidoreductases nitrite oxidoreductase (NxrAB), nitrite reductase (NirK), ammonia monooxygenase (AmoABC), manganese oxidase (MnxG), formate dehydrogenase (FdoGH and FDH), and carbon monoxide dehydrogenase (CoxLM) displayed distributions indicative of biogeochemical status such as oxidative or nutritional stress, with the potential to be more sensitive than chemical sensors. Enzymes that mediate transformations of atmospheric gases like CO, CO 2 , NO, methanethiol, and methylamines were most abundant in the upwelling region. We identified hot spots of biochemical transformation in the central Pacific Ocean, highlighted previously understudied metabolic pathways in the environment, and provided rich empirical data for biogeochemical models critical for forecasting ecosystem response to climate change.

Dataset: ProteOMZ Exclusive Peptide Level Spectral Counts, Relative protein abundance from scaled and corrected exclusive peptide spectral counts from 20-1250 m in the water column (0.2-3 µm filter size fraction) from the ProteOMZ R/V Falkor expedition. There are a total of 107,579 unique peptide sequences from 56,543 protein groups (88,251 proteins). Exclusive spectral counts are provided per sample as are the full dataset scaled and normalized spectral counts. The protein distributions in this dataset highlight the microbial dynamics across biomes in the central Pacific Ocean. These data were submitted in Saunders et al. (2022). For a complete list of measurements, refer to the full dataset description in the supplemental file 'Dataset_description.pdf'. The most current version of this dataset is available at: https://www.bco-dmo.org/dataset/868030, Gordon and Betty Moore Foundation: Marine Microbiology Initiative (MMI) GBMF3782, Schmidt Ocean Institute (SOI) R/V Falkor 160115 SOI ProteOMZ Expedition