Heterotrophic bacteria in the ocean invest carbon, nitrogen, and energy in extracellular enzymes to hydrolyze large substrates to smaller sizes suitable for uptake. Since hydrolysis products produced outside of a cell may be lost to diffusion, the return on this investment is uncertain. Selfish bacteria change the odds in their favor by binding, partially hydrolyzing, and transporting polysaccharides into the periplasmic space without loss of hydrolysis products. We expected selfish bacteria to be most common in the upper ocean, where phytoplankton produce abundant fresh organic matter, including complex polysaccharides. We, therefore, sampled water in the western North Atlantic Ocean at four depths from three stations differing in physiochemical conditions; these stations and depths also differed considerably in microbial community composition. To our surprise, we found that selfish bacteria are common throughout the water column of the ocean, including at depths greater than 5500 m. Selfish uptake as a strategy thus appears to be geographically—and phylogenetically—widespread. Since processing and uptake of polysaccharides require enzymes that are highly sensitive to substrate structure, the activities of these bacteria might not be reflected by measurements relying on uptake only of low molecular weight substrates. Moreover, even at the bottom of the ocean, the supply of structurally-intact polysaccharides, and therefore the return on enzymatic investment, must be sufficient to maintain these organisms.

Abstract. Oceanic bacterial communities process a major fraction of marine organic carbon. A substantial portion of this carbon transformation occurs in the mesopelagic zone, and a further fraction fuels 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 (0–200 m), mesopelagic (200–1000 m), and bathypelagic (1000–4000 m) 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 to the input of HMW organic matter – 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: as bacterial community composition changed in response to the addition of HMW organic matter, the rate and spectrum of enzymatic activities increased. In epipelagic mesocosms, the spectrum of peptidase activities became especially broad and glucosidase activities were very high, a pattern not seen at other depths, which, in contrast, were dominated by leucine aminopeptidase and had much lower peptidase and glucosidase rates in general. 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.

Heterotrophic bacteria use extracellular enzymes to hydrolyze high molecular weight (HMW) organic matter to low molecular weight (LMW) hydrolysis products that can be taken into the cell. These enzymes represent a considerable investment of carbon, nitrogen, and energy, yet the return on this investment is uncertain, since hydrolysis of a HMW substrate outside a cell yields LMW products that can be lost to diffusion and taken up by scavengers that do not produce extracellular enzymes1. However, an additional strategy of HMW organic matter utilization, selfish uptake2, is used for polysaccharide degradation, and has recently been found to be widespread among bacterial communities in surface ocean waters3. During selfish uptake, polysaccharides are bound at the cell surface, initially hydrolyzed, and transported into the periplasmic space without loss of hydrolysis products2, thereby retaining hydrolysate for the selfish bacteria and reducing availability of LMW substrates to scavenging bacteria. Here we show that selfish bacteria are common not only in the sunlit upper ocean, where polysaccharides are freshly produced by phytoplankton, but also deeper in the oceanic water column, including in bottom waters at depths of more than 5,500 meters. Thus, the return on investment, and therefore also the supply of suitable polysaccharides, must be sufficient to maintain these organisms.

Heterotrophic bacteria initiate the degradation of high molecular weight organic matter by producing an array of extracellular enzymes to hydrolyze complex organic matter into sizes that can be taken up into the cell. These bacterial communities differ spatially and temporally in composition, and potentially also in their enzymatic complements. Previous research has shown that particle-associated bacteria can be considerably more active than bacteria in the surrounding bulk water, but most prior studies of particle-associated bacteria have been focused on the upper ocean - there are few measurements of enzymatic activities of particle-associated bacteria in the mesopelagic and bathypelagic ocean, although the bacterial communities in the deep are dependent upon degradation of particulate organic matter to fuel their metabolism. We used a broad suite of substrates to compare the glucosidase, peptidase, and polysaccharide hydrolase activities of particle-associated and unfiltered seawater microbial communities in epipelagic, mesopelagic, and bathypelagic waters across 11 stations in the western North Atlantic. We concurrently determined bacterial community composition of unfiltered seawater and of samples collected via gravity filtration (>3 μm). Overall, particle-associated bacterial communities showed a broader spectrum of enzyme activities compared with unfiltered seawater communities. These differences in enzymatic activities were greater at offshore than at coastal locations, and increased with increasing depth in the ocean. The greater differences in enzymatic function measured on particles with depth coincided with increasing differences in particle-associated community composition, suggesting that particles act as ‘specialty centers’ that are essential for degradation of organic matter even at bathypelagic depths.

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