Exopolymer Microdomains as a Structuring Agent for Heterogeneity Within Microbial Biofilms

Abstract

It is now well-recognized that the majority, and often most active fractions, of microbial cells in many natural systems occur as surface-associated biofilms. In sedimentary environments, biofilm formation represents an important functional adaptation for microbial life. At the level of an individual sediment particle, the biofilm community represents a cacophony of cellular and extracellular processes enclosed within an amorphous biofilm. Recent studies using new analytical approaches now suggest that the seemingly amorphous biofilm instead may be a highly structured system, one in which microbial cells actively manipulate their extracellular polymers and overall microenvironment to accomplish specific tasks. At microspatial scales (nanometers to micrometers), biofilm polymers are important in sequestering of nutrients, localization of extracellular enzymes, and providing a protective and stabilizing microenvironment for cells. Examination of the three-dimensional nature of microbial biofilm communities and activities through the use of nuclear magnetic resonance (NMR) spectroscopy, confocal laser microscopy (CLM), atomic-force microscopy (AFM) and other techniques are beginning to provide quantitative evidence for microscale partitioning within biofilms. In light of these new data, the biofilm is explored here as an important structural matrix to partition microbial extracellular activities and effectively promote heterogeneity over very small (i.e., molecular) spatial scales. Structuring and partitioning may occur through the formation of “exopolymer-mediated microdomains.” These are regions of a biofilm matrix where specific types of exopolymers are concentrated and impart unique physical/chemical properties to the biofilm. Accumulating evidence, derived from isotope sorption studies, electron microscopy, and CLM supports this idea. The presence of exopolymer microdomains may provide microorganisms with a structuring mechanism to spatially segregate extracellular activities over small spatial scales.