Giving structure to the biofilm matrix: an overview of individual strategies and emerging common themes

Abstract

Biofilms are communities of microbial cells that underpin diverse processes including sewage bioremediation, plant growth promotion, chronic infections and industrial biofouling. The cells resident in the biofilm are encased within a self-produced exopolymeric matrix that commonly comprises lipids, proteins that frequently exhibit amyloid-like properties, eDNA and exopolysaccharides. This matrix fulfils a variety of functions for the community, from providing structural rigidity and protection from the external environment to controlling gene regulation and nutrient adsorption. Critical to the development of novel strategies to control biofilm infections, or the capability to capitalize on the power of biofilm formation for industrial and biotechnological uses, is an in-depth knowledge of the biofilm matrix. This is with respect to the structure of the individual components, the nature of the interactions between the molecules and the three-dimensional spatial organization. We highlight recent advances in the understanding of the structural and functional role that carbohydrates and proteins play within the biofilm matrix to provide three-dimensional architectural integrity and functionality to the biofilm community. We highlight, where relevant, experimental techniques that are allowing the boundaries of our understanding of the biofilm matrix to be extended using Escherichia coli, Staphylococcus aureus, Vibrio cholerae, and Bacillus subtilis as exemplars.

Pathogen-mediated manipulation of arthropod microbiota to promote infection

“…Similarities in the relative abundance of Enterococci within the tick gut, found by microbiome analysis or SEM imaging of tick gut biofilms when treated with D-serine, to those during A. phagocytophilum infection or P1 injection of tick guts support the mechanistic action of IAFGP's peptidoglycan binding activity on modulating the tick microbiota. D-amino acids interfere with the linking of biofilm adhesion proteins, and with cell wall remodeling (51)(52)(53)(54). Therefore, we hypothesized that IAFGP binding to peptidoglycan could cause alterations in bacterial physiology and morphology that would reduce the ability of Gram-positive bacteria to form tenacious biofilms-adversely affecting the relative composition of the gut microbiota.…”

Architectural transitions in Vibrio cholerae biofilms at single-cell resolution

“…Because of their ubiquity and their relevance to medicine and industry, the formation of biofilms has been studied intensively, with an emphasis on the genes, regulatory mechanisms, and transport properties that underlie transitions from planktonic growth to surface attachment (15)(16)(17), to proliferation and matrix secretion (2,18), and finally to dispersal (19,20). A basic understanding of several regulatory circuits and secreted matrix components governing biofilm formation has been developed (21)(22)(23)(24)(25). Nonetheless, the physical, biological, and chemical factors that interact to determine the biofilm architecture remain largely unknown.…”

Vibrio cholerae biofilm growth program and architecture revealed by single-cell live imaging

“…On the other hand, biofilms can be useful, for example, in waste-water treatment (7). Investigations have focused on the genetic and regulatory features driving biofilm formation and on defining the composition of the extracellular matrix (8). However, still lacking is a fundamental biophysical understanding of how bacteria, in time and space, build these 3D structures that attach to surfaces and resist mechanical and chemical perturbations.…”

“…One common assumption is that bacteria produce polymeric matrices that expand the volume occupied by cells and carry them into the third dimension, as demonstrated by many computer simulations (9,10). Matrix proteins, extracellular DNA, lipids, and bacteriophages have also been shown to influence the formation of the overall biofilm structure (8). However, the role the bacterial cells themselves play in shaping the biofilm architecture has not been widely investigated; hence, many basic questions remain.…”