Microbial Community Drivers in Anaerobic Granulation at High Salinity

Microbial cells (i.e., bacteria, archaea, microeukaryotes) in oceans secrete a diverse array of large molecules, collectively called extracellular polymeric substances (EPSs) or simply exopolymers. These secretions facilitate attachment to surfaces that lead to the formation of structured ‘biofilm’ communities. In open-water environments, they also lead to formation of organic colloids, and larger aggregations of cells, called ‘marine snow.’ Secretion of EPS is now recognized as a fundamental microbial adaptation, occurring under many environmental conditions, and one that influences many ocean processes. This relatively recent realization has revolutionized our understanding of microbial impacts on ocean systems. EPS occur in a range of molecular sizes, conformations and physical/chemical properties, and polysaccharides, proteins, lipids, and even nucleic acids are actively secreted components. Interestingly, however, the physical ultrastructure of how individual EPS interact with each other is poorly understood. Together, the EPS matrix molecules form a three-dimensional architecture from which cells may localize extracellular activities and conduct cooperative/antagonistic interactions that cannot be accomplished efficiently by free-living cells. EPS alter optical signatures of sediments and seawater, and are involved in biogeomineral precipitation and the construction of microbial macrostructures, and horizontal-transfers of genetic information. In the water-column, they contribute to the formation of marine snow, transparent exopolymer particles (TEPs), sea-surface microlayer biofilm, and marine oil snow. Excessive production of EPS occurs during later-stages of phytoplankton blooms as an excess metabolic by product and releases a carbon pool that transitions among dissolved-, colloidal-, and gel-states. Some EPS are highly labile carbon forms, while other forms appear quite refractory to degradation. Emerging studies suggest that EPS contribute to efficient trophic-transfer of environmental contaminants, and may provide a protective refugia for pathogenic cells within marine systems; one that enhances their survival/persistence. Finally, these secretions are prominent in ‘extreme’ environments ranging from sea-ice communities to hypersaline systems to the high-temperatures/pressures of hydrothermal-vent systems. This overview summarizes some of the roles of exopolymer in oceans.

Bacterial biofilms are organized communities of cells living in association with surfaces. The hallmark of biofilm formation is the secretion of a polymeric matrix rich in sugars and proteins in the extracellular space. In Bacillus subtilis, secretion of the exopolysaccharide (EPS) component of the extracellular matrix is genetically coupled to the inhibition of flagella-mediated motility. The onset of this switch results in slow expansion of the biofilm on a substrate. Different strains have radically different capabilities in surface colonization: Flagella-null strains spread at the same rate as wild type, while both are dramatically faster than EPS mutants. Multiple functions have been attributed to the EPS, but none of these provides a physical mechanism for generating spreading. We propose that the secretion of EPS drives surface motility by generating osmotic pressure gradients in the extracellular space. A simple mathematical model based on the physics of polymer solutions shows quantitative agreement with experimental measurements of biofilm growth, thickening, and spreading. We discuss the implications of this osmotically driven type of surface motility for nutrient uptake that may elucidate the reduced fitness of the matrix-deficient mutant strains.