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  1. Abstract

    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.

     
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  2. 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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  3. Abstract. Oceanic bacterial communities process a major fraction of marine organiccarbon. A substantial portion of this carbon transformation occurs in themesopelagic zone, and a further fraction fuels bacteria in the bathypelagiczone. However, the capabilities and limitations of the diverse microbialcommunities at these depths to degrade high-molecular-weight (HMW) organicmatter are not well constrained. Here, we compared the responses of distinctmicrobial communities from North Atlantic epipelagic (0–200 m), mesopelagic(200–1000 m), and bathypelagic (1000–4000 m) waters at two open-oceanstations to the same input of diatom-derived HMW particulate and dissolvedorganic matter. Microbial community composition and functional responses tothe input of HMW organic matter – as measured by polysaccharide hydrolase,glucosidase, and peptidase activities – were very similar between thestations, which were separated by 1370 km but showed distinct patterns withdepth. Changes in microbial community composition coincided with changes inenzymatic activities: as bacterial community composition changed in responseto the addition of HMW organic matter, the rate and spectrum of enzymaticactivities increased. In epipelagic mesocosms, the spectrum of peptidaseactivities became especially broad and glucosidase activities were veryhigh, a pattern not seen at other depths, which, in contrast, were dominatedby leucine aminopeptidase and had much lower peptidase and glucosidase ratesin general. The spectrum of polysaccharide hydrolase activities was enhancedparticularly in epipelagic and mesopelagic mesocosms, with fewerenhancements in rates or spectrum in bathypelagic waters. The timing andmagnitude of these distinct functional responses to the same HMW organicmatter varied with depth. Our results highlight the importance of residencetimes at specific depths in determining the nature and quantity of organicmatter reaching the deep sea. 
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  4. Abstract

    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.

     
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  5. Summary

    The extent to which differences in microbial community structure result in variations in organic matter (OM) degradation is not well understood. Here, we tested the hypothesis that distinct marine microbial communities from North Atlantic surface and bottom waters would exhibit varying compositional succession and functional shifts in response to the same pool of complex high molecular weight (HMW‐OM). We also hypothesized that microbial communities would produce a broader spectrum of enzymes upon exposure to HMW‐OM, indicating a greater potential to degrade these compounds than reflected by initial enzymatic activities. Our results show that community succession in amended mesocosms was congruent with cell growth, increased bacterial production and most notably, with substantial shifts in enzymatic activities. In all amended mesocosms, closely related taxa that were initially rare became dominant at time frames during which a broader spectrum of active enzymes were detected compared to initial timepoints, indicating a similar response among different communities. However, succession on the whole‐community level, and the rates, spectra and progression of enzymatic activities, reveal robust differences among distinct communities from discrete water masses. These results underscore the crucial role of rare bacterial taxa in ocean carbon cycling and the importance of bacterial community structure for HMW‐OM degradation.

     
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