Metaproteomics reveals differential modes of metabolic coupling among ubiquitous oxygen minimum zone microbes

Abstract

Marine oxygen minimum zones (OMZs) are intrinsic water column features arising from respiratory oxygen demand during organic matter degradation in stratified waters. Currently OMZs are expanding due to global climate change with resulting feedback on marine ecosystem function. Here we use metaproteomics to chart spatial and temporal patterns of gene expression along defined redox gradients in a seasonally stratified fjord to better understand microbial community responses to OMZ expansion. The expression of metabolic pathway components for nitrification, anaerobic ammonium oxidation (anammox), denitrification, and inorganic carbon fixation were differentially expressed across the redoxcline and covaried with distribution patterns of ubiquitous OMZ microbes including Thaumarchaeota, Nitrospina, Nitrospira, Planctomycetes, and SUP05/ARCTIC96BD-19 Gammaproteobacteria. Nitrification and inorganic carbon fixation pathways affiliated with Thaumarchaeota dominated dysoxic waters, and denitrification, sulfur oxidation, and inorganic carbon fixation pathways affiliated with the SUP05 group of nitrate-reducing sulfur oxidizers dominated suboxic and anoxic waters. Nitrifier nitrite oxidation and anammox pathways affiliated with Nirospina, Nitrospira, and Planctomycetes, respectively, also exhibited redox partitioning between dysoxic and suboxic waters. The numerical abundance of SUP05 proteins mediating inorganic carbon fixation under anoxic conditions suggests that SUP05 will become increasingly important in global ocean carbon and nutrient cycling as OMZs expand.

Fig. 1.

Hierarchical clustering of metaproteome by NSAF (see Methods) for detected proteins from Sep09 S2, S3, and S4 indicating compartments of the water column, with adjacent sparklines for oxygen (O₂), nitrate (NO₃⁻), and hydrogen sulfide (H₂S) for each sample.

Fig. 2.

Distribution and NSAF value of proteins involved in nitrogen and sulfur-based energy metabolism and inorganic carbon fixation for taxa abundant in the metaproteome. For metagenome (gray, Apr08 only) and metaproteome in upper oxycline (green), lower oxycline (teal), S/N transition zone (blue), and sulfidic zone (purple). See Table S4 for full list of protein names; Anx indicates anammox hydroxylamine oxidoreductase and hydrazine oxidoreductase proteins.

Fig. 3.

Relative abundance of SUP05 genes and proteins in two overlapping SUP05 fosmid sequences (GQ351266 and GQ351267) (16). Metagenome (gray, Apr08 only) and metaproteome for the upper oxycline (green), lower oxycline (teal), S/N transition zone (blue), and sulfidic zone (purple). Selected SUP05 genes involved in denitrification (dark gray shading), sulfide oxidation (black shading), and putative hydroxylamine oxidoreductase (diagonal lines) are indicated. Protein abundance shown as summed NSAF values for all detected ORFs with top hit to a given SUP05 protein. Metagenome abundances shown as percentage of ORFs with top hit to a given SUP05 gene with sparklines for oxygen (O₂), nitrate (NO₃⁻), and hydrogen sulfide (H₂S) for each sample.

Fig. 4.

Proposed metabolic model based on metaproteomic observations for heterotrophic remineralization (brown) and energetic coupling (yellow dashed lines) of nitrogen (green), sulfur (red), and hydrogen (orange) based chemolithotrophic energy metabolism with carbon fixation (yellow star) for taxa abundant in the metaproteome. Line weight and arrow size indicate magnitude of metabolic activity. Gray lines, activity not occurring under given conditions; light gray taxa, reduced abundance and metabolic activity.