From molecules to multispecies ecosystems: the roles of structure in bacterial biofilms

Abstract

Biofilms are communities of sessile microbes that are bound to each other by a matrix made of biopolymers and proteins. Spatial structure is present in biofilms on many lengthscales. These range from the nanometer scale of molecular motifs to the hundred-micron scale of multicellular aggregates. Spatial structure is a physical property that impacts the biology of biofilms in many ways. The molecular structure of matrix components controls their interaction with each other (thereby impacting biofilm mechanics) and with diffusing molecules such as antibiotics and immune factors (thereby impacting antibiotic tolerance and evasion of the immune system). The size and structure of multicellular aggregates, combined with microbial consumption of growth substrate, give rise to differentiated microenvironments with different patterns of metabolism and gene expression. Spatial association of more than one species can benefit one or both species, while distances between species can both determine and result from the transport of diffusible factors between species. Thus, a widespread theme in the biological importance of spatial structure in biofilms is the effect of structure on transport. We survey what is known about this and other effects of spatial structure in biofilms, from molecules up to multispecies ecosystems. We conclude with an overview of what experimental approaches have been developed to control spatial structure in biofilms and how these and other experiments can be complemented with computational work.

Effect of N-Acetylcysteine in Combination with Antibiotics on the Biofilms of Three Cystic Fibrosis Pathogens of Emerging Importance

“…Biofilm matrices are composed of extracellular polymers (EPS) comprising microbially produced polysaccharides, extracellular-DNA and proteins [2]. Biofilm formation provides resistance to shear stress and tolerance to antibiotics in biotic environments [3], thereby promoting chronic infection.…”

Engineering controllable biofilms for biotechnological applications

“…The maintenance of long‐term robustness and stable interactions among community members is necessary to facilitate the deployment of engineered multispecies biofilms in complex bioprocesses (Johns et al ., 2016). The spatial arrangement of different species within multispecies biofilm and cell‐to‐cell interactions plays a major role in building a stable community (Kim et al ., 2008; Johns et al ., 2016; Gordon et al ., 2019). Spatial distribution of different microorganisms within a multispecies biofilm promotes population survival by producing public goods, facilitating interactions between different species and enhancing community resilience to environmental perturbations (Lee et al ., 2014; Johns et al ., 2016).…”

Neutralization of ionic interactions by dextran-based single-chain nanoparticles improves tobramycin diffusion into a mature biofilm

“…Alginate protects bacteria from the immune system by inhibiting the complement system and reducing phagocytosis by neutrophils and macrophages. Together with eDNA, this negatively charged polysaccharide binds to a positively charged antibiotic, thus diminishing antibiotic diffusion throughout the biofilm 18 – 20 .…”