The virulence regulatorbvgSis required for nutrient-induced filamentation inBordetella avium

Bacteria can change morphology in response to stressors and changes in their environment, including infection of a host. We previously identified the bacterial species,Bordetella atropi, which uses nutrient-induced filamentation as a novel mechanism for cell-to-cell spreading in the intestinal epithelial cells of a nematode host. To further investigate the conservation of nutrient-induced filamentation in Bordetellae, we utilized the turkey-infecting speciesBordetella aviumwhich filaments in vitro when switched from a standard growth media to an enriched media. We conducted a selection-based filamentation screen withB. aviumand isolated two independent non-filamentous mutants that failed to filament in highly enriched media. These mutants contained different alleles inbvgS, the sensor in the two-component master virulence regulator (BvgAS) conserved across the Bordetella genus. To investigate the role ofbvgSin nutrient-induced filamentation, we conducted transcriptomics and found thatbvgSmutation resulted in loss of responsiveness to highly-enriched media, especially in genes related to nutrient uptake and metabolism. The most dysregulated gene in thebvgSmutant encoded for succinyl-CoA:acetate CoA-transferase (SCACT) and we were able to regulate filamentation with exogenous metabolites up and downstream of this enzyme. These data suggest thatbvgSregulates nutrient-induced filamentation by controlling metabolic capacity. Overall, we found that the virulence regulatorbvgSis required for nutrient-induced filamentation inB. avium, suggesting there may be conservation in Bordetellae for utilizing this morphological change as a virulence phenotype.