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SAR86 is an abundant and ubiquitous heterotroph in the surface ocean that plays a central role in the function of marine ecosystems. We hypothesized that despite its ubiquity, different SAR86 subgroups may be endemic to specific ocean regions and functionally specialized for unique marine environments. However, the global biogeographical distributions of SAR86 genes, and the manner in which these distributions correlate with marine environments, have not been investigated. We quantified SAR86 gene content across globally distributed metagenomic samples and modeled these gene distributions as a function of 51 environmental variables. We identified five distinct clusters of genes within the SAR86 pangenome, each with a unique geographic distribution associated with specific environmental characteristics. Gene clusters are characterized by the strong taxonomic enrichment of distinct SAR86 genomes and partial assemblies, as well as differential enrichment of certain functional groups, suggesting differing functional and ecological roles of SAR86 ecotypes. We then leveraged our models and high-resolution, remote sensing-derived environmental data to predict the distributions of SAR86 gene clusters across the world's oceans, creating global maps of SAR86 ecotype distributions. Our results reveal that SAR86 exhibits previously unknown, complex biogeography, and provide a framework for exploring geographic distributions of genetic diversity from other microbial clades.

Heterotrophic bacteria in the ocean initiate biopolymer degradation using extracellular enzymes that yield low molecular weight hydrolysis products in the environment, or by using a selfish uptake mechanism that retains the hydrolysate for the enzyme‐producing cell. The mechanism used affects the availability of hydrolysis products to other bacteria, and thus also potentially the composition and activity of the community. In marine systems, these two mechanisms of substrate processing have been studied in the water column, but to date, have not been investigated in sediments. In surface sediments from an Arctic fjord of Svalbard, we investigated mechanisms of biopolymer hydrolysis using four polysaccharides and mucin, a glycoprotein. Extracellular hydrolysis of all biopolymers was rapid. Moreover, rapid degradation of mucin suggests that it may be a key substrate for benthic microbes. Although selfish uptake is common in ocean waters, only a small fraction (0.5%–2%) of microbes adhering to sediments used this mechanism. Selfish uptake was carried out primarily by Planctomycetota and Verrucomicrobiota. The overall dominance of extracellular hydrolysis in sediments, however, suggests that the bulk of biopolymer processing is carried out by a benthic community relying on the sharing of enzymatic capabilities and scavenging of public goods. [ABSTRACT FROM AUTHOR]

Heterotrophic bacteria process nearly half of the organic matter produced by phytoplankton in the surface ocean. Much of this organic matter consists of high molecular weight (HMW) biopolymers such as polysaccharides and proteins, which must initially be hydrolyzed to smaller sizes by structurally specific extracellular enzymes. To assess the relationships between substrate structure and microbial community composition and function, we concurrently determined carbohydrate abundance and structural complexity, bacterial community composition, and peptidase and polysaccharide hydrolase activities throughout the water column at four distinct stations in the western North Atlantic Ocean. Although the monosaccharide constituents of particulate organic matter (POM) were similar among stations, the structural complexity of POM-derived polysaccharides varied by depth and station, as demonstrated by polysaccharide-specific antibody probing. Bacterial community composition and polysaccharide hydrolase activities also varied by depth and station, suggesting that the structure and function of bacterial communities—and the structural complexity of their target substrates—are interlinked. Thus, the extent to which bacteria can transform organic matter in the ocean is dependent on both the structural complexity of the organic matter and their enzymatic capabilities in different depths and regions of the ocean. [ABSTRACT FROM AUTHOR]

Heterotrophic bacteria hydrolyze high molecular weight (HMW) organic matter extracellularly prior to uptake, resulting in diffusive loss of hydrolysis products. An alternative 'selfish' uptake mechanism that minimises this loss has recently been found to be common in the ocean. We investigated how HMW organic matter addition affects these two processing mechanisms in surface and bottom waters at three stations in the North Atlantic Ocean. A pulse of HMW organic matter increased cell numbers, as well as the rate and spectrum of extracellular enzymatic activities at both depths. The effects on selfish uptake were more differentiated: in Gulf Stream surface waters and productive surface waters south of Newfoundland, selfish uptake of structurally simple polysaccharides increased upon HMW organic matter addition. The number of selfish bacteria taking up structurally complex polysaccharides, however, was largely unchanged. In contrast, in the oligotrophic North Atlantic gyre, despite high external hydrolysis rates, the number of selfish bacteria was unchanged, irrespective of polysaccharide structure. In deep bottom waters (> 4000 m), structurally complex substrates were processed only by selfish bacteria. Mechanisms of substrate processing—and the extent to which hydrolysis products are released to the external environment—depend on substrate structural complexity and the resident bacterial community. [ABSTRACT FROM AUTHOR]

Oceanic bacterial communities process a major fraction of marine organic carbon, with a substantial portion of this carbon transformation occurring in the mesopelagic zone, and a further fraction fueling bacteria in the bathypelagic zone. However, the capabilities and limitations of the diverse microbial communities at these depths to degrade high molecular weight (HMW) organic matter are not well constrained. Here, we compared the responses of distinct microbial communities from North Atlantic epipelagic, mesopelagic, and bathypelagic waters at two open ocean stations to the same input of diatom-derived HMW particulate and dissolved organic matter. Microbial community composition and functional responses – as measured by polysaccharide hydrolase, glucosidase, and peptidase activities – were very similar between the stations, which were separated by 1370 km, but showed distinct patterns with depth. Changes in microbial community composition coincided with changes in enzymatic activities. In epipelagic mesocosms, the spectrum of peptidase activities became especially broad and glucosidase activities were very high, a pattern not seen at other depths. The spectrum of polysaccharide hydrolase activities was enhanced particularly in epipelagic and mesopelagic mesocosms, with fewer enhancements in rates or spectrum in bathypelagic waters. The timing and magnitude of these distinct functional responses to the same HMW organic matter varied with depth. Our results highlight the importance of residence times at specific depths in determining the nature and quantity of organic matter reaching the deep sea. [ABSTRACT FROM AUTHOR]