Selfish bacteria are active throughout the water column of the ocean

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.

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

“…Moreover, at both depths, HMW organic matter addition also fueled considerable bacterial growth (Figures 1 and 2). Furthermore, the observation that an enhancement in the supply of natural organic matter during a spring bloom fueled a similar response—enhancement only of selfish laminarin uptake—concurrent with widespread external hydrolysis (Giljan et al, 2023; Reintjes, Fuchs, Scharfe, et al, 2020), suggests that the responses observed in the mesocosm experiments are not an anomaly.…”

“…Extensive selfish uptake of laminarin by Bacteroidota has previously been measured during the late stages of a phytoplankton bloom in the North Sea (Reintjes, Fuchs, Scharfe, et al, 2020). Selfish Planctomycetes have been identified in the surface waters of the Atlantic Ocean (Reintjes et al, 2017), while Verrucomicrobiota , in particular the clade Pedosphaeraceae , showed strong selfish uptake of laminarin in early summer in the North Sea (Giljan et al, 2023). Here, we found that increases in the abundance of selfish bacteria capable of laminarin uptake in amended mesocosms were occasionally the result of increases in a singular group, which varied by treatment, depth, and station.…”

“…Based on bacterial community composition data, Giljan et al (2023) suggested that the ability to selfishly take up FLA‐PS is phylogenetically widespread because the unamended mesocosms show a relatively constant percent of selfish bacteria against a backdrop of changing community composition. Our FISH results, which provide the first identification of selfish bacteria capable of laminarin uptake in the bathypelagic ocean, support this hypothesis.…”

“…Our study shows that the mechanisms by which heterotrophic bacterial communities respond to these changes are affected by the nature of the specific substrate that they process (Figure 7), as well as by the composition and capabilities of the starting community. Selfish uptake, as a substrate processing mechanism, is phylogenetically widespread and occurs throughout the water column (Figures 1–3 and 6; Giljan et al, 2023). The observation that selfish bacteria that utilise more complex substrates (e.g., arabinogalactan and fucoidan especially at Stn.…”

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

“…Balmonte et al ., 2018; Reintjes et al ., 2020b). Recently, serendipitous observations of fluorescently stained cells in incubations with FLA‐PS demonstrated that the selfish mechanism plays an important role in ocean surface waters (Reintjes et al ., 2017, 2019, 2020a & 2020b) and even in the deep ocean (Giljan et al ., 2021). Either or both of these mechanisms could be used by the heterotrophic community to degrade a given polysaccharide, but the extent to which one is used can vary greatly (e.g.…”