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Shared biophysical mechanisms determine early biofilm architecture development across different bacterial species.

ABSTRACT: Bacterial biofilms are among the most abundant multicellular structures on Earth and play essential roles in a wide range of ecological, medical, and industrial processes. However, general principles that govern the emergence of biofilm architecture across different species remain unknown. Here, we combine experiments, simulations, and statistical analysis to identify shared biophysical mechanisms that determine early biofilm architecture development at the single-cell level, for the species Vibrio cholerae, Escherichia coli, Salmonella enterica, and Pseudomonas aeruginosa grown as microcolonies in flow chambers. Our data-driven analysis reveals that despite the many molecular differences between these species, the biofilm architecture differences can be described by only 2 control parameters: cellular aspect ratio and cell density. Further experiments using single-species mutants for which the cell aspect ratio and the cell density are systematically varied, and mechanistic simulations show that tuning these 2 control parameters reproduces biofilm architectures of different species. Altogether, our results show that biofilm microcolony architecture is determined by mechanical cell-cell interactions, which are conserved across different species.

SUBMITTER: Jeckel H

PROVIDER: S-EPMC9605341 | biostudies-literature | 2022 Oct

REPOSITORIES: biostudies-literature

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Shared biophysical mechanisms determine early biofilm architecture development across different bacterial species.

Jeckel Hannah H Díaz-Pascual Francisco F Skinner Dominic J DJ Song Boya B Jiménez-Siebert Eva E Strenger Kerstin K Jelli Eric E Vaidya Sanika S Dunkel Jörn J Drescher Knut K

PLoS biology 20221026 10

Bacterial biofilms are among the most abundant multicellular structures on Earth and play essential roles in a wide range of ecological, medical, and industrial processes. However, general principles that govern the emergence of biofilm architecture across different species remain unknown. Here, we combine experiments, simulations, and statistical analysis to identify shared biophysical mechanisms that determine early biofilm architecture development at the single-cell level, for the species Vib ...[more]

PMID: 36288405

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Project description:Chronic infections caused by polymicrobial biofilms are often difficult to treat effectively, partially due to the elevated tolerance of polymicrobial biofilms to antimicrobial treatments. It is known that interspecific interactions influence polymicrobial biofilm formation. However, the underlying role of the coexistence of bacterial species in polymicrobial biofilm formation is not fully understood. Here, we investigated the effect of the coexistence of Enterococcus faecalis, Escherichia coli O157:H7, and Salmonella enteritidis on triple-species biofilm formation. Our results demonstrated that the coexistence of these three species enhanced the biofilm biomass and led to restructuring of the biofilm into a tower-like architecture. Furthermore, the proportions of polysaccharides, proteins, and eDNAs in the extracellular matrix (ECM) composition of the triple-species biofilm were significantly changed compared to those in the E. faecalis mono-species biofilm. Finally, we analyzed the transcriptomic profile of E. faecalis in response to coexistence with E. coli and S. enteritidis in the triple-species biofilm. The results suggested that E. faecalis established dominance and restructured the triple-species biofilm by enhancing nutrient transport and biosynthesis of amino acids, upregulating central carbon metabolism, manipulating the microenvironment through "biological weapons," and activating versatile stress response regulators. Together, the results of this pilot study reveal the nature of E. faecalis-harboring triple-species biofilms with a static biofilm model and provide novel insights for further understanding interspecies interactions and the clinical treatment of polymicrobial biofilms. IMPORTANCE Bacterial biofilms possess distinct community properties that affect various aspects of our daily lives. In particular, biofilms exhibit increased tolerance to chemical disinfectants, antimicrobial agents, and host immune responses. Multispecies biofilms are undoubtedly the dominant form of biofilms in nature. Thus, there is a pressing need for more research directed at delineating the nature of multispecies biofilms and the effects of the properties on the development and survival of the biofilm community. Here, we address the effects of the coexistence of Enterococcus faecalis, Escherichia coli, and Salmonella enteritidis on triple-species biofilm formation with a static model. In combination with transcriptomic analyses, this pilot study explores the potential underlying mechanisms that lead to the dominance of E. faecalis in triple-species biofilms. Our findings provide novel insights into the nature of triple-species biofilms and indicate that the composition of multispecies biofilms should be a key consideration when determining antimicrobial treatments.

Project description:Numerous ecological interactions among microbes-for example, competition for space and resources, or interaction among phages and their bacterial hosts-are likely to occur simultaneously in multispecies biofilm communities. While biofilms formed by just a single species occur, multispecies biofilms are thought to be more typical of microbial communities in the natural environment. Previous work has shown that multispecies biofilms can increase, decrease, or have no measurable impact on phage exposure of a host bacterium living alongside another species that the phages cannot target. The reasons underlying this variability are not well understood, and how phage-host encounters change within multispecies biofilms remains mostly unexplored at the cellular spatial scale. Here, we study how the cellular scale architecture of model 2-species biofilms impacts cell-cell and cell-phage interactions controlling larger scale population and community dynamics. Our system consists of dual culture biofilms of Escherichia coli and Vibrio cholerae under exposure to T7 phages, which we study using microfluidic culture, high-resolution confocal microscopy imaging, and detailed image analysis. As shown previously, sufficiently mature biofilms of E. coli can protect themselves from phage exposure via their curli matrix. Before this stage of biofilm structural maturity, E. coli is highly susceptible to phages; however, we show that these bacteria can gain lasting protection against phage exposure if they have become embedded in the bottom layers of highly packed groups of V. cholerae in co-culture. This protection, in turn, is dependent on the cell packing architecture controlled by V. cholerae biofilm matrix secretion. In this manner, E. coli cells that are otherwise susceptible to phage-mediated killing can survive phage exposure in the absence of de novo resistance evolution. While co-culture biofilm formation with V. cholerae can confer phage protection to E. coli, it comes at the cost of competing with V. cholerae and a disruption of normal curli-mediated protection for E. coli even in dual species biofilms grown over long time scales. This work highlights the critical importance of studying multispecies biofilm architecture and its influence on the community dynamics of bacteria and phages.

Dataset Information

Shared biophysical mechanisms determine early biofilm architecture development across different bacterial species.

Publications

Shared biophysical mechanisms determine early biofilm architecture development across different bacterial species.

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