Intercellular collectivity is governed by enzyme secretion strategies in marine polysaccharide degrading bacteria

Abstract

Polysaccharide breakdown by bacteria requires the activity of enzymes that degrade polymers extracellularly. This generates a localized pool of breakdown products that are accessible to the enzyme producers themselves as well as to other organisms. Marine bacterial taxa often show marked differences in the production and secretion of degradative enzymes that break down polysaccharides. These differences can have profound effects on the pool of diffusible breakdown products and hence on the ecological dynamics. However, the consequences of differences in enzymatic secretions on cellular growth dynamics and interactions are unclear. Here we combine experiments and models to study the growth dynamics of single cells within populations of marine Vibrionaceae strains that grow on the abundant marine polymer alginate, using microfluidics coupled to quantitative single-cell analysis and mathematical modelling. We find that strains that have low extracellular secretions of alginate lyases show stronger aggregative behaviors compared to strains that secrete high levels of enzymes. One plausible reason for this observation is that low secretors require a higher cellular density to achieve maximal growth rates in comparison with high secretors. Our findings indicate that increased aggregation increases intercellular synergy amongst cells of low-secreting strains. By mathematically modelling the impact of the level of degradative enzyme secretion on the rate of oligomer loss to diffusion, we find that enzymatic capability modulates the propensity of cells within clonal populations to cooperate or compete with each other. Our experiments and models demonstrate that marine bacteria display distinct aggregative behaviors and intercellular interactions based on their enzymatic secretion capabilities when growing on polysaccharides.

Effects of interspecies interactions on marine community ecosystem function

“…In microbial systems that rely on polymer degradation for nutrient availability, growth and enzyme production are tightly coupled (24, 25). Increases in hydrolytic enzyme production and activity were found to lead to increased cell growth; furthermore, the number of degrading cells tends to be positively correlated with the amount of enzymes produced.…”

“…Our observations of gene expression changes in the presence of Alteromonas are in line with previous studies that show that growth behaviour on carbohydrate polymers such as aggregation or dispersal and the production of hydrolytic enzymes are tightly coupled (36). A study performed with various Vibrio species on the polymer alginate has shown that the presence of cross-feeders changes the aggregation of the degrading species (24). In combination, these findings suggest that secreted extracellular chitinases might provide two functions to the degraders.…”

Interspecies interactions determine growth dynamics of biopolymer degrading populations in microbial communities

“…Yellow Since the presence of cross-feeders alters the growth dynamics of degrader cells it is plausible that the activity of alginate lyases, enzymes that mediate breakdown of alginate, is also altered. In ZF270 cells, alginate lyases are secreted extracellularly (17). Therefore, quantifying the activity of alginate lyases enabled the measurement of the effect of cross-feeders on the enzyme activity of degraders.…”

“…Therefore, the number of cells and their positioning within microfluidic chambers is determined by the cellular growth rate as well as by cell movement (18). ZF270 cells are known to form aggregates when growing on alginate in microfluidic growth chambers (17) and the increased local cell density due to aggregation allows cells to cooperatively degrade alginate. In accordance with previous findings, we found that ZF270 cells form aggregates when growing on alginate (Figure 3A, Supplemental Video 1).…”

“…Degrader cells often aggregate while growing on polysaccharides like chitin (14), alginate (15)(16)(17) or xylan (4,18). Previous experimental and computational studies have established that aggregation, by increasing local cell density, allows degrader cells to benefit from the polysaccharide breakdown activities of neighboring cells (4,15,19).…”