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Abstract Heterotrophic microbes are central to organic matter degradation and transformation in marine sediments. Currently, most investigations of benthic microbiomes do not differentiate between processes in the porewater and on the grains and, hence, only show a generalized picture of the community. This limits our understanding of the structure and functions of sediment microbiomes. To address this problem, we fractionated sandy surface sediment microbial communities from a coastal site in Isfjorden, Svalbard, into cells associated with the porewater, loosely attached to grains, and firmly attached to grains; we found dissimilar bacterial communities and metabolic activities in these fractions. Most (84%–89%) of the cells were firmly attached, and this fraction comprised more anaerobes, such as sulfate reducers, than the other fractions. The porewater and loosely attached fractions (3% and 8%–13% of cells, respectively) had more aerobic heterotrophs. These two fractions generally showed a higher frequency of dividing cells, polysaccharide (laminarin) hydrolysis rates, and per-cell O2 consumption than the firmly attached cells. Thus, the different fractions occupy distinct niches within surface sediments: the firmly attached fraction is potentially made of cells colonizing areas on the grain that are protected from abrasion, but might be more diffusion-limited for organic matter and electron acceptors. In contrast, the porewater and loosely attached fractions are less resource-limited and have faster growth. Their cell numbers are kept low possibly through abrasion and exposure to grazers. Differences in community composition and activity of these cell fractions point to their distinct roles and contributions to carbon cycling within surface sediments. 

Abstract 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 byPlanctomycetotaandVerrucomicrobiota. 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 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 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. 

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. 

Microbe-mediated enzymatic hydrolysis of organic matter entails the production of hydrolysate, the recovery of which may be more or less efficient. The selfish uptake mechanism, recently discovered, allows microbes to hydrolyze polysaccharides and take up large oligomers, which are then degraded in the periplasmic space. By minimizing the hydrolysate loss, selfish behaviour may be profitable for free-living cells dwelling in a patchy substrate landscape. However, selfish uptake seems to be tailored to algal-derived polysaccharides, abundant in organic particles, suggesting that particle-attached microbes may use this strategy. We tracked selfish polysaccharides uptake in surface microbial communities of the northeastern Mediterranean Sea, linking the occurrence of this processing mode with microbial lifestyle. Additionally, we set up fluorescently labelled polysaccharides incubations supplying phytodetritus to investigate a ‘pioneer’ scenario for particle-attached microbes. Under both conditions, selfish behaviour was almost exclusively carried out by particle-attached microbes, suggesting that this mechanism may represent an advantage in the race for particle exploitation. Our findings shed light on the selfish potential of particle-attached microbes, suggesting multifaceted foraging strategies exerted by particle colonizers. 

Extracellular enzyme activity is a well-established parameter for evaluating microbial biogeochemical roles in marine ecosystems. The presence and activity of extracellular enzymes in seawater provide insights into the quality and quantity of organic matter being processed by the present microorganisms. A key challenge in our understanding of these processes is to decode the extracellular enzyme repertoire and activities of natural communities at the single-cell level. Current measurements are carried out on bulk or size-fractionated samples capturing activities of mixed populations. This approach – even with size-fractionation – cannot be used to trace enzymes back to their producers, nor distinguish the active microbial members, leading to a disconnect between measured activities and the producer cells. By targeting extracellular enzymes and resolving their activities at the single-cell level, we can investigate underlying phenotypic heterogeneity among clonal or closely related organisms, characterize enzyme kinetics under varying environmental conditions, and resolve spatio-temporal distribution of individual enzyme producers within natural communities. In this perspective piece, we discuss state-of-the-art technologies in the fields of microfluidic droplets and functional screening of prokaryotic cells for measuring enzyme activity in marine seawater samples, one cell at a time. We further elaborate on how this single-cell approach can be used to address research questions that cannot be answered with current methods, as pertinent to the enzymatic degradation of organic matter by marine microorganisms.