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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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Linking lifestyle and foraging strategies of marine bacteria: selfish behaviour of particle‐attached bacteria in the northern Adriatic Sea
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.
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- PAR ID:
- 10338564
- Date Published:
- Journal Name:
- Environmental Microbiology Reports
- ISSN:
- 1758-2229
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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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.more » « less
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Abstract Heterotrophic microorganisms are responsible for transforming and respiring a substantial fraction of the organic matter produced by phytoplankton in the surface ocean. Much of this organic matter is composed of polysaccharides, high‐molecular weight (HMW) sugars. To initiate degradation of polysaccharides, microorganisms must produce extracellular enzymes of the right structural specificity to hydrolyze these complex structures. To date, most measurements of enzyme activities are made at in situ temperatures, but at atmospheric pressure. However, previous studies have shown that hydrostatic pressure can impact the functionality of enzymes. Since deep sea communities may be seeded by microbes from shallow waters, we aimed to determine if pressure affects the performance of enzymes from coastal waters. To determine the extent to which enzymatic activities of coastal microbial communities are affected by pressure, we quantified the degradation of seven polysaccharides under pressures ranging from 0.1 MPa (atmospheric) to 40 MPa (equivalent to 4,000 m). Enzyme activities of pelagic communities were inhibited with increased pressure, while enzyme activities of benthic microbial communities were more resistant to increased pressure. Addition of HMW organic matter resulted in communities with enzyme activities that were more resistant to increased pressure. However, the freely‐dissolved enzymes (<0.2 μm) produced by these communities were strongly inhibited by increased hydrostatic pressure, suggesting that the pressure‐resistant enzymes were cell‐surface attached. Because pressure inhibition of enzyme activities varied strongly by polysaccharide, we surmise that the structural complexity of a polysaccharide—and therefore the number of distinct enzymes required for hydrolysis—is likely closely associated with pressure inhibition.more » « less
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Accepted Manuscript
- Journal Article:
- https://doi.org/10.1111/1758-2229.13059
