Institute of Biogeochemistry and Pollutant Dynamics, Department of Environmental Systems Science, ETH Zurich, Zurich, Switzerland; Department of Environmental Microbiology, Eawag: Swiss Federal Institute of Aquatic Science and Technology, Dübendorf, Switzerland; Geological Institute, Department of Earth Sciences, ETH Zurich, Zurich, Switzerland
Department of Civil and Environmental Engineering, MIT, Cambridge, United States; Department of Biology, University of Southern California, Los Angeles, United States
Sammy Pontrelli
Institute of Molecular Systems Biology, Department of Biology, ETH Zurich, Zurich, Switzerland
Estelle E Clerc
Institute of Environmental Engineering, Department of Civil, Environmental and Geomatic Engineering, ETH Zurich, Zurich, Switzerland
Samuel Charlton
Institute of Environmental Engineering, Department of Civil, Environmental and Geomatic Engineering, ETH Zurich, Zurich, Switzerland
Roman Stocker
Institute of Environmental Engineering, Department of Civil, Environmental and Geomatic Engineering, ETH Zurich, Zurich, Switzerland
Cara Magnabosco
Geological Institute, Department of Earth Sciences, ETH Zurich, Zurich, Switzerland
Institute of Biogeochemistry and Pollutant Dynamics, Department of Environmental Systems Science, ETH Zurich, Zurich, Switzerland; Department of Environmental Microbiology, Eawag: Swiss Federal Institute of Aquatic Science and Technology, Dübendorf, Switzerland
Institute of Biogeochemistry and Pollutant Dynamics, Department of Environmental Systems Science, ETH Zurich, Zurich, Switzerland; Department of Environmental Microbiology, Eawag: Swiss Federal Institute of Aquatic Science and Technology, Dübendorf, Switzerland; Laboratory of Microbial Systems Ecology, School of Architecture, Civil and Environmental Engineering (ENAC), École Polytechnique Fédéral de Lausanne (EPFL), Lausanne, Switzerland
Institute of Biogeochemistry and Pollutant Dynamics, Department of Environmental Systems Science, ETH Zurich, Zurich, Switzerland; Department of Environmental Microbiology, Eawag: Swiss Federal Institute of Aquatic Science and Technology, Dübendorf, Switzerland
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 bacterium Vibrio cyclitrophicus ZF270 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.
