Polysaccharide breakdown products drive degradation-dispersal cycles of foraging bacteria through changes in metabolism and motility
Authors: Stubbusch Astrid K.M. , Keegstra Johannes M. , Schwartzman Julia , Pontrelli Sammy , Clerc Estelle E. , Charlton Samuel , Stocker Roman , Magnabosco Cara , Schubert Olga T. , Ackermann Martin , D’Souza Glen G. 
Published: July 2023

Most of Earth’s biomass is composed of polysaccharides. During biomass decomposition, polysaccharides are degraded by heterotrophic bacteria as a nutrient and energy source and are thereby partly remineralized into CO2. As polysaccharides are heterogeneously distributed in nature, following the colonization and degradation of a polysaccharide hotspot the cells need to reach new polysaccharide hotspots. Even though many studies indicate that these degradation-dispersal cycles contribute to the carbon flow in marine systems, we know little about how cells alternate between polysaccharide degradation and motility, and which environmental factors trigger this behavioral switch. Here, we studied the growth of the marine bacteriumVibrio cyclitrophicusZF270 on the abundant marine polysaccharide alginate, both in its soluble polymeric form as well as on its breakdown products. We used microfluidics coupled to time-lapse microscopy to analyze motility and growth of individual cells, and RNA sequencing to study associated changes in gene expression. We found that single cells grow at reduced rate on alginate until they form large groups that cooperatively break down the polymer. Exposing cell groups to digested alginate accelerates cell growth and changes the expression of genes involved in alginate degradation and catabolism, central metabolism, ribosomal biosynthesis, and transport. However, exposure to digested alginate also triggers cells to become motile and disperse from cell groups, proportionally increasing with the group size before the nutrient switch, and this is accompanied by high expression of genes involved in flagellar assembly, chemotaxis, and quorum sensing. The motile cells chemotax toward polymeric but not digested alginate, likely enabling them to find new polysaccharide hotspots. Overall, our findings reveal cellular mechanisms that might also underlie bacterial degradation-dispersal cycles, which influence the remineralization of biomass in marine environments.

Importance

Polysaccharides, also known as glycans, are the most abundant form of biomass on Earth and understanding how they are degraded by microorganisms is essential for our understanding of the global carbon cycle and the storage and release of CO2by natural systems. Although group formation is a common strategy used by bacterial cells to degrade ubiquitous polymeric growth substrates in nature, where nutrient hotspots are heterogeneously distributed, little is known about how cells prepare for dispersal from an exhausted nutrient source and re-initiate degradation of new nutrient patches. By quantifying growth, motility and chemotaxis of individual cells and comparing gene expression changes when populations were exposed to either polysaccharides or their degradation products in the form of digested polysaccharides, we show that bacterial cells alter their behavior when they experience a shift from polymeric to digested polysaccharides: After cells form groups during growth on polymers, the exposure to degradation products triggered cells to become motile, enabling dispersal from sessile cell groups. The chemotactic attraction of motile cells to polymeric alginate likely allows cells to move towards new polysaccharide hotspots. Our study sheds light on the cellular processes that drive bacterial growth and behavior during carbon remineralization, an important process resulting in CO2release from natural systems.