Metaproteomic analysis of a winter to spring succession in coastal northwest Atlantic Ocean microbial plankton

Abstract

In this study, we used comparative metaproteomics to investigate the metabolic activity of microbial plankton inhabiting a seasonally hypoxic basin in the Northwest Atlantic Ocean (Bedford Basin). From winter to spring, we observed a seasonal increase in high-affinity membrane transport proteins involved in scavenging of organic substrates; Rhodobacterales transporters were strongly associated with the spring phytoplankton bloom, whereas SAR11 transporters were abundant in the underlying waters. A diverse array of transporters for organic compounds were similar to the SAR324 clade, revealing an active heterotrophic lifestyle in coastal waters. Proteins involved in methanol oxidation (from the OM43 clade) and carbon monoxide (from a wide variety of bacteria) were identified throughout Bedford Basin. Metabolic niche partitioning between the SUP05 and ARCTIC96BD-19 clades, which together comprise the Gamma-proteobacterial sulfur oxidizers group was apparent. ARCTIC96BD-19 proteins involved in the transport of organic compounds indicated that in productive coastal waters this lineage tends toward a heterotrophic metabolism. In contrast, the identification of sulfur oxidation proteins from SUP05 indicated the use of reduced sulfur as an energy source in hypoxic bottom water. We identified an abundance of Marine Group I Thaumarchaeota proteins in the hypoxic deep layer, including proteins for nitrification and carbon fixation. No transporters for organic compounds were detected among the thaumarchaeal proteins, suggesting a reliance on autotrophic carbon assimilation. In summary, our analyses revealed the spatiotemporal structure of numerous metabolic activities in the coastal ocean that are central to carbon, nitrogen and sulfur cycling in the sea.

Figure 1

Physicochemical conditions in Bedford Basin over the time-frame relevant to this study. (a) Temperature, (b) salinity (PSU, Practical Salinity Units), (c) oxygen and (d) fluorescence. Stars represent the location of the samples used for metaproteomic analysis.

Figure 2

Taxonomic composition of the Bedford Basin bacterial community based on 16S rRNA gene sequences.

Figure 3

Taxonomic composition of identified proteins in Bedford Basin metaproteomes based on spectral counts.

Figure 4

Functional composition of identified proteins in Bedford metaproteomes based on spectral counts. Proteins within the transporter COG categories (E, G, P and Q) were differentiated into those specifically involved in transport function and those involved in the intracellular metabolism of transported solutes.

Figure 5

The relative abundance of solute transport proteins identified in Bedford Basin metaproteomes based on spectra counts.