Polysaccharide breakdown products drive degradation-dispersal cycles of foraging bacteria through changes in metabolism and motility

Abstract

AbstractMost 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 these degradation-dispersal cycles are an integral part in the global carbon cycle, we know little about how cells alternate between 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. We used microfluidics-coupled time-lapse microscopy to analyze motility and growth of individual cells, and RNA sequencing to study associated changes in gene expression. 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, accompanied by high expression of genes involved in flagellar assembly, chemotaxis, and quorum sensing. The motile cells chemotax toward alginate hotspots, likely enabling cells to find new polysaccharide hotspots. Overall, our findings reveal the cellular mechanisms underlying bacterial degradation-dispersal cycles that drive remineralization in natural environments.ImportancePolysaccharides, 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 made cells motile, enabling dispersal from sessile cell groups and - guided by chemotaxis - movement towards new polysaccharide hotspots. Our study sheds light on the cellular processes that drive bacterial growth and behavior during carbon remineralization, an important driver of CO2release from biomass in natural systems.