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

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.

Keywords: Sargasso Sea; amino acids; bacterioplankton; dissolved organic matter; metabolites; mixing; seasonal.

FIGURE 1

ODV contour plots of (A) temperature (solid white line represents monthly maximum mixed layer depth (MLD) and the colored bar on top represents seasons), (B) dissolved organic carbon (DOC) concentration, (C) total dissolved amino acid carbon (TDAA C) concentration, (D) degradation index (DI) from TDAA, (E) bacterioplankton abundance (BA), and (F) apparent oxygen utilization (AOU) from July 2016 to September 2017 over the surface 300 m of northwestern Sargasso Sea. Red dashed rectangle indicates the general timing of deep convective mixing, and white dashed rectangle at 120–300 m defines the upper mesopelagic zone.

FIGURE 2

Comparison of upper mesopelagic (120–300 m) mean temperature, dissolved organic carbon (DOC), total dissolved amino acid carbon (TDAA C), degradation index (DI), bacterioplankton abundance (BA), and apparent oxygen utilization (AOU) between mixed season and other seasons (including spring transition, stratified, and fall transition) from July 2016 to September 2017. Bars represent mean with standard error and asterisk (*) designates significant differences between the periods (unpaired t-test, p < 0.05).

FIGURE 3

Patterns of production or loss of metabolites in the mixed layer over the seasonal cycle. Green areas indicate the net loss of a metabolite relative to conservative mixing in that time-period compared to the previous month, blue areas indicate net production of a metabolite relative to conservative mixing, while gray areas indicate metabolite concentration changes were solely due to mixing. Metabolite categories are shown as different colors besides the metabolite names. These categories are not exclusive; Supplementary Table 2 lists the categories shown here as well as additional categories. The statistical methods (described in methods) determined that the metabolite pattern in April (max mixing) was different from other time periods.

FIGURE 4

Vertical profile of ³H-Leucine incorporation rates, a proxy for bacterial production (BP), over the surface 300 m during cruises in (A) July 2016, (B) September 2016, (C) April 2017, and (D) July 2017. Data points represent the average of replicates and error bars are standard error. The red dashed line (120 m) separates the euphotic zone from the upper mesopelagic zone. Red arrows indicate enhancement of BP in the mesopelagic zone during mixing in April 2017 compared to other stratified periods.

FIGURE 5

(A) Non-metric multi-dimensional scaling (NMDS) plot showing first two axes of all 16S amplicon sequence variants (ASVs) color coded by depths and shaped by seasons over July 2016 to Sept 2017. The five points in the bottom part of the NMDS plot came from the same cast in July 2017. We cannot explain the driver of these five outliers, nor could we identify a reason to remove them; thus, they are included in the plot. (B) Simprof cluster analysis of bacterial community structures at 160 and 200 m. Different clusters are shown at 70% dissimilarity threshold. Samples names are in color bar and symbols next to each sample name indicate season with symbol shapes as defined in (A).

FIGURE 6

ODV contour plots of the ASV relative abundance (%) in the surface 300 m for bacterioplankton lineages in the (A) SAR11 clade, (B) SAR202 clade, (C) Flavobacteriaceae NS4 marine group, (D) SAR86 clade, (E) Acidimicrobiales OM1 clade, and (F) SAR406 clade that showed enrichment in the mesopelagic zone during or shortly after mixing events and that were significantly positively cross-correlated with DOC and/or TDAA C with negative lag within July 2016 to September 2017 time frame. Red dashed rectangle indicates convective mixing time frame during this time period and white dashed rectangle indicates 120–300 m of the upper mesopelagic zone.

FIGURE 7

Anomaly between observed mean relative abundance between mesopelagic 120–300 m during and shortly following maximal mixing (April 2017 to July 2017) and mean mesopelagic 120–300 m relative abundance during the entire study period for representative ASVs in the (A) SAR11 clade, (B) SAR202 clade, (C) Flavobacteriaceae NS4 marine group, (D) SAR86 clade, (E) Acidimicrobiales OM1 clade, and (F) SAR406 clade as shown in Figure 6. Blue solid lines and dashed lines indicate zero and ± one standard deviation of all-time data, respectively. Data points above zero suggest enrichment of that ASV during or shortly after mixing. Arrow indicates max MLD time.