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ABSTRACT 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 avium,which filamentsin vitrowhen 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 theBordetellagenus. To investigate the role ofbvgSin nutrient-induced filamentation, we conducted transcriptomics and found that our allele ofbvgSresulted 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, 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 regulatorbvgScan control nutrient-induced filamentation inB. avium,suggesting there may be conservation in Bordetellae for utilizing this morphological change as a virulence phenotype.IMPORTANCEBordetella aviumis the causative agent of bordetellosis, an infectious disease affecting the respiratory system of birds, significantly increasing morbidity in poultry, ultimately leading to economic losses. It is long known that the pathogenesis ofB. aviumis governed by the two-component master virulence regulator, BvgAS. However, this regulon has never before been associated with nutrient-induced filamentation. In this study, we identify BvgS to be regulating nutrient-induced filamentation. We also report the first transcriptomics analysis of filamentousB. avium, showing the enzyme succinyl-CoA:acetate CoA-transferase may be involved in a metabolic shift in enriched nutrient conditions leading to filamentation. Our results suggest that virulence inB. aviumis a dynamic relationship, affected by nutrient availability, rather than a simple binary decision.