Pulsed inputs of high molecular weight organic matter shift the mechanisms of substrate utilisation in marine bacterial communities.

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.

Selfish bacteria are active throughout the water column of the ocean.

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.

Strong seasonal differences of bacterial polysaccharide utilization in the North Sea over an annual cycle.

Marine heterotrophic bacteria contribute considerably to global carbon cycling, in part by utilizing phytoplankton-derived polysaccharides. The patterns and rates of two different polysaccharide utilization modes - extracellular hydrolysis and selfish uptake - have previously been found to change during spring phytoplankton bloom events. Here we investigated seasonal changes in bacterial utilization of three polysaccharides, laminarin, xylan and chondroitin sulfate. Strong seasonal differences were apparent in mode and speed of polysaccharide utilization, as well as in bacterial community compositions. Compared to the winter month of February, during the spring bloom in May, polysaccharide utilization was detected earlier in the incubations and a higher portion of all bacteria took up laminarin selfishly. Highest polysaccharide utilization was measured in June and September, mediated by bacterial communities that were significantly different from spring assemblages. Extensive selfish laminarin uptake, for example, was detectible within a few hours in June, while extracellular hydrolysis of chondroitin was dominant in September. In addition to the well-known Bacteroidota and Gammaproteobacteria clades, the numerically minor verrucomicrobial clade Pedosphaeraceae could be identified as a rapid laminarin utilizer. In summary, polysaccharide utilization proved highly variable over the seasons, both in mode and speed, and also by the bacterial clades involved.

Metabolism of a hybrid algal galactan by members of the human gut microbiome.

Native porphyran is a hybrid of porphryan and agarose. As a common element of edible seaweed, this algal galactan is a frequent component of the human diet. Bacterial members of the human gut microbiota have acquired polysaccharide utilization loci (PULs) that enable the metabolism of porphyran or agarose. However, the molecular mechanisms that underlie the deconstruction and use of native porphyran remains incompletely defined. Here, we have studied two human gut bacteria, porphyranolytic Bacteroides plebeius and agarolytic Bacteroides uniformis, that target native porphyran. This reveals an exo-based cycle of porphyran depolymerization that incorporates a keystone sulfatase. In both PULs this cycle also works together with a PUL-encoded agarose depolymerizing machinery to synergistically reduce native porphyran to monosaccharides. This provides a framework for understanding the deconstruction of a hybrid algal galactan, and insight into the competitive and/or syntrophic relationship of gut microbiota members that target rare nutrients.

Bacterioplankton reveal years-long retention of Atlantic deep-ocean water by the Tropic Seamount.

Seamounts, often rising hundreds of metres above surrounding seafloor, obstruct the flow of deep-ocean water. While the retention of deep-water by seamounts is predicted from ocean circulation models, its empirical validation has been hampered by large scale and slow rate of the interaction. To overcome these limitations we use the growth of planktonic bacteria to assess the retention time of deep-ocean water by a seamount. The selected Tropic Seamount in the North-Eastern Atlantic is representative for the majority of isolated seamounts, which do not affect the surface ocean waters. We prove deep-water is retained by the seamount by measuring 2.4× higher bacterial concentrations in the seamount-associated or 'sheath'-water than in deep-ocean water unaffected by seamounts. Genomic analyses of flow-sorted, dominant sheath-water bacteria confirm their planktonic origin, whilst proteomic analyses of the sheath-water bacteria, isotopically labelled in situ, indicate their slow growth. According to our radiotracer experiments, it takes the sheath-water bacterioplankton 1.5 years to double their concentration. Therefore, the seamount should retain the deep-ocean water for 1.8 years for the deep-ocean bacterioplankton to grow to the 2.4× higher concentration in the sheath-water. We propose that turbulent mixing of the seamount sheath-water stimulates bacterioplankton growth by increasing cell encounter rate with ambient dissolved organic molecules.