Extensive cellular multi-tasking within Bacillus subtilis biofilms

Yannarell, Sarah M.; Beaudoin, Eric S.; Talley, Hunter S.; Schoenborn, Alexi A.; Orr, Galya; Anderton, Christopher R.; Chrisler, William B.; Shank, Elizabeth A.

doi:10.1128/msystems.00891-22

Extensive cellular multi-tasking within Bacillus subtilis biofilms

Journal Article · Tue Aug 01 00:00:00 EDT 2023 · mSystems

DOI:https://doi.org/10.1128/msystems.00891-22· OSTI ID:2204039

^[1]; ^[2]; ^[1]; ^[1]; ^[3]; ^[3]; Chrisler, William B. ^[3]; ^[2]

University of North Carolina, Chapel Hill, NC (United States)
University of Massachusetts Chan Medical School, Worcester, MA (United States)
Pacific Northwest National Laboratory (PNNL), Richland, WA (United States)

Bacillus subtilis is a soil-dwelling bacterium that can form biofilms, or communities of cells surrounded by a self-produced extracellular matrix. In biofilms, genetically identical cells often exhibit heterogeneous transcriptional phenotypes, so that subpopulations of cells carry out essential yet costly cellular processes that allow the entire population to thrive. Surprisingly, the extent of phenotypic heterogeneity and the relationships between subpopulations of cells within biofilms of even in well-studied bacterial systems like B. subtilis remains largely unknown. To determine relationships between these subpopulations of cells, we created 182 strains containing pairwise combinations of fluorescent transcriptional reporters for the expression state of 14 different genes associated with potential cellular subpopulations. We determined the spatial organization of the expression of these genes within biofilms using confocal microscopy, which revealed that many reporters localized to distinct areas of the biofilm, some of which were co-localized. We used flow cytometry to quantify reporter co-expression, which revealed that many cells “multi-task,” simultaneously expressing two reporters. These data indicate that prior models describing B. subtilis cells as differentiating into specific cell types, each with a specific task or function, were oversimplified. Only a few subpopulations of cells, including surfactin and plipastatin producers, as well as sporulating and competent cells, appear to have distinct roles based on the set of genes examined here. These data will provide us with a framework with which to further study and make predictions about the roles of diverse cellular phenotypes in B. subtilis biofilms.

View Accepted Manuscript (DOE)

Research Organization:: Oak Ridge Institute for Science and Education (ORISE), Oak Ridge, TN (United States); Pacific Northwest National Laboratory (PNNL), Richland, WA (United States)

Sponsoring Organization:: National Institutes of Health (NIH); USDOE Office of Science (SC), Biological and Environmental Research (BER); USDOE Office of Science (SC), Office of Workforce Development for Teachers & Scientists (WDTS)

Grant/Contract Number:: AC05-76RL01830; SC0014664

OSTI ID:: 2204039

Report Number(s):: PNNL-SA--182983

Journal Information:: mSystems, Journal Name: mSystems Journal Issue: 4 Vol. 8; ISSN 2379-5077

Publisher:: American Society for MicrobiologyCopyright Statement

Country of Publication:: United States

Language:: English

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