Linkages Among Dissolved Organic Matter Export, Dissolved Metabolites, and Associated Microbial Community Structure Response in the Northwestern Sargasso Sea on a Seasonal Scale.

Elizabeth B Kujawinski,Ruth Curry,Shuting Liu,Dennis A Hansell,Kevin Vergin,Craig A Carlson,Krista Longnecker,Rod Johnson,Stephen J Giovannoni,Elisa Halewood,Luis M Bolaños,Rachel Parsons,Keri Opalk

doi:10.3389/fmicb.2022.833252

Abstract

Deep convective mixing of dissolved and suspended organic matter from the surface to depth can represent an important export pathway of the biological carbon pump. The seasonally oligotrophic Sargasso Sea experiences annual winter convective mixing to as deep as 300 m, providing a unique model system to examine dissolved organic matter (DOM) export and its subsequent compositional transformation by microbial oxidation. We analyzed biogeochemical and microbial parameters collected from the northwestern Sargasso Sea, including bulk dissolved organic carbon (DOC), total dissolved amino acids (TDAA), dissolved metabolites, bacterial abundance and production, and bacterial community structure, to assess the fate and compositional transformation of DOM by microbes on a seasonal time-scale in 2016–2017. DOM dynamics at the Bermuda Atlantic Time-series Study site followed a general annual trend of DOC accumulation in the surface during stratified periods followed by downward flux during winter convective mixing. Changes in the amino acid concentrations and compositions provide useful indices of diagenetic alteration of DOM. TDAA concentrations and degradation indices increased in the mesopelagic zone during mixing, indicating the export of a relatively less diagenetically altered (i.e., more labile) DOM. During periods of deep mixing, a unique subset of dissolved metabolites, such as amino acids, vitamins, and benzoic acids, was produced or lost. DOM export and compositional change were accompanied by mesopelagic bacterial growth and response of specific bacterial lineages in the SAR11, SAR202, and SAR86 clades, Acidimicrobiales, and Flavobacteria, during and shortly following deep mixing. Complementary DOM biogeochemistry and microbial measurements revealed seasonal changes in DOM composition and diagenetic state, highlighting microbial alteration of the quantity and quality of DOM in the ocean.

Highlights

Marine dissolved organic matter (DOM) is produced by various food-web processes such as extracellular release from phytoplankton, zooplankton excretion, grazer sloppy feeding, bacterial release, and viral lysis (Carlson and Hansell, 2015; Koch et al, 2020)
Microbial oxidation leads to compositional changes of DOM that can be assessed by examining changes in specific components, such as dissolved combined neutral sugars (DCNS) (Skoog and Benner, 1997; Goldberg et al, 2009) or total dissolved amino acids (TDAA)
Dynamics of Dissolved Organic Carbon The seasonal variability of dissolved inorganic nutrients, chlorophyll fluorescence, particulate organic matter2,3 and dissolved organic matter observed during this study are consistent with seasonal cycles of hydrography and organic carbon dynamics previously observed in this region (Hansell and Carlson, 2001; Steinberg et al, 2001; Lomas et al, 2013)

Summary

Introduction

Marine dissolved organic matter (DOM) is produced by various food-web processes such as extracellular release from phytoplankton, zooplankton excretion, grazer sloppy feeding, bacterial release, and viral lysis (Carlson and Hansell, 2015; Koch et al, 2020). A portion of freshly produced dissolved organic carbon (DOC) from phytoplankton was drawn down rapidly within 1–2 weeks in the Southern Ocean and Arctic Ocean, selecting for a distinct bacterial community structure (Landa et al, 2018; Dadaglio et al, 2019); in contrast, a majority of DOC in the water column is composed of compounds of varying degrees of recalcitrance that turn over on a time scale of months to millennia (Carlson and Ducklow, 1995; Hansell, 2013; Carlson and Hansell, 2015). Microbial oxidation leads to compositional changes of DOM that can be assessed by examining changes in specific components, such as dissolved combined neutral sugars (DCNS) (Skoog and Benner, 1997; Goldberg et al, 2009) or total dissolved amino acids (TDAA). A commonly used degradation index (DI) is calculated with each amino acid’s relative abundance and its empirical factor coefficient; this index is sensitive to DOM degradation over time scales of weeks to decades (Dauwe et al, 1999; Davis et al, 2009; Kaiser and Benner, 2009)

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Conclusion