Unique inducible filamentous motility identified in pathogenic Bacillus cereus group species

Authors: LIU, MARTHA - University Of British Columbia; COLEMAN, SHANNON - University Of British Columbia; WILKINSON, LAUREN - University Of British Columbia; SMITH, MAREN - University Of British Columbia; HOANG, THOMAS - University Of British Columbia; NIYAH, NAOMI - Pennsylvania State University; MUKHERJEE, MANJARI - Pennsylvania State University; Huynh, Steven; Parker, Craig; KOVAC, JASNA - Pennsylvania State University; HANCOCK, ROBERT - University Of British Columbia; GAYNOR, ERIN - University Of British Columbia

Submitted to: The ISME Journal: Multidisciplinary Journal of Microbial Ecology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 7/23/2020
Publication Date: 8/7/2020
Citation: Liu, M.M., Coleman, S., Wilkinson, L., Smith, M.L., Hoang, T., Niyah, N., Mukherjee, M., Huynh, S., Parker, C., Kovac, J., Hancock, R., Gaynor, E.C. 2020. Unique inducible filamentous motility identified in pathogenic Bacillus cereus group species. The ISME Journal: Multidisciplinary Journal of Microbial Ecology. 14:2997–3010. https://doi.org/10.1038/s41396-020-0728-x.
DOI: https://doi.org/10.1038/s41396-020-0728-x

Interpretive Summary: Bacterial surface migration is increasingly being recognized as an important aspect of bacterial fitness by allowing cells to sense and occupy new niches, translocate rapidly across surfaces, resist antibiotics and other deleterious circumstances, and shift virulence states. We isolated an atmospheric contaminant, subsequently identified as a new strain of Bacillus mobilis, which showed a unique, robust, rapid, and inducible filamentous surface motility. This flagella-independent motility was characterized by formation of elongated cells at the expanding edge, and was induced when cells were inoculated onto lawns of metabolically inactive Campylobacter jejuni cells, autoclaved bacterial biomass, adsorbed milk, and adsorbed blood atop hard agar plates. Phosphatidylcholine (PC), bacterial membrane components, and sterile human fecal extracts were also sufficient to induce filamentous expansion. Screening of eight other Bacillus spp. showed that filamentous motility was conserved amongst B. cereus group species to varying degrees. RNA-Seq of elongated expanding cells collected from adsorbed milk and PC lawns compared to control rod-shaped cells revealed dysregulation of genes involved in metabolism and membrane transport, sporulation, quorum sensing, antibiotic synthesis, and virulence (e.g., hblA/B/C/D and plcR). These findings characterize the robustness and potential importance of filamentous surface motility in B. cereus group species and lay the foundation for understanding the biological role it may have during host colonization including the contribution to bacterial success and colonization in host intestinal systems.

Technical Abstract: Active migration across semi-solid surfaces is important for bacterial success by facilitating colonization of unoccupied niches and is often associated with altered virulence and antibiotic resistance profiles. We isolated an atmospheric contaminant, subsequently identified as a new strain of Bacillus mobilis, which showed a unique, robust, rapid, and inducible filamentous surface motility. This flagella-independent motility was characterized by formation of elongated cells at the expanding edge, and was induced when cells were inoculated onto lawns of metabolically inactive Campylobacter jejuni cells, autoclaved bacterial biomass, adsorbed milk, and adsorbed blood atop hard agar plates. Phosphatidylcholine (PC), bacterial membrane components, and sterile human fecal extracts were also sufficient to induce filamentous expansion. Screening of eight other Bacillus spp. showed that filamentous motility was conserved amongst B. cereus group species to varying degrees. RNA-Seq of elongated expanding cells collected from adsorbed milk and PC lawns compared to control rod-shaped cells revealed dysregulation of genes involved in metabolism and membrane transport, sporulation, quorum sensing, antibiotic synthesis, and virulence (e.g., hblA/B/C/D and plcR). These findings characterize the robustness and potential importance of filamentous surface motility in B. cereus group species and lay the foundation for understanding the biological role it may have during host colonization.