A starvation-induced regulator, RovM, acts as a switch for planktonic/biofilm state transition in Yersinia pseudotuberculosis

Abstract

The transition between the planktonic state and the biofilm-associated state is a key developmental decision for pathogenic bacteria. Biofilm formation by Yersinia pestis is regulated by hmsHFRS genes (β-1, 6-N-acetyl-D-glucosamine synthesis operon) in its flea vector and in vitro. However, the mechanism of biofilm formation in Yersinia pseudotuberculosis remains elusive. In this study, we demonstrate that the LysR-type regulator RovM inversely regulates biofilm formation and motility in Y. pseudotuberculosis by acting as a transcriptional regulator of these two functions. RovM is strongly induced during growth in minimal media but strongly repressed in complex media. On one hand, RovM enhances bacterial motility by activating the expression of FlhDC, the master regulator of flagellar genes, via the recognition of an operator upstream of the flhDC promoter. On the other hand, RovM represses β-GlcNAc production under nutrition-limited conditions, negatively regulating hmsHFRS expression by directly binding to the −35 element of its promoter. Compared to wild-type bacteria, the rovM mutant established denser biofilms and caused more extensive mortality in mice and silkworm larvae. These results indicate that RovM acts as a molecular switch to coordinate the expression of genes involved in biofilm formation and motility in response to the availability of nutrients.

An Osmoregulatory Mechanism Operating through OmpR and LrhA Controls the Motile-Sessile Switch in the Plant Growth-Promoting Bacterium Pantoea alhagi

“…These results suggest that LrhA negatively regulates flhDC expression by directly binding to the flhDC promoter. Consistent with the master regulatory role of FlhD 4 C 2 in flagellar biosynthesis and motility (10,40), there was no motility observed in the ΔflhDC mutant or the ΔlrhA ΔflhDC double mutant ( Fig. 1B).…”

“…Therefore, bacteria have evolved a variety of strategies to control the multistep process of cell motility to avoid inappropriate energy expenditure (2,10,57). Previous studies have shown that LrhA and its homologues play a positive or negative role in bacterial motility mainly through controlling the expression of the flagellar master operon flhDC at the transcriptional level (33,35,40). Consistent with the role of LrhA in E. coli but opposite to that in Xenorhabdus nematophila (32,33,35), our results indicate that LrhA in P. alhagi represses flagellar motility by directly inhibiting the transcription of flhDC.…”

Bacterial glycogen provides short-term benefits in changing environments

“…The latter is unlikely as our previous experiments have indicated metabolic, viable activity for cells well into starvation. Biofilm formation is induced by nutrient starvation and inhibited by glucose addition (Thomason, Fontaine, De Lay, & Storz, 2012; Zhao et al, 2017). We therefore reason that glycogen facilitates the attachment phase of biofilm formation under starvation conditions, here by providing resources for matrix protein or flagella production.…”

The Yersinia pseudotuberculosis Cpx envelope stress system contributes to transcriptional activation of rovM

“…Second, transcriptome analyses of CpxR-regulated genes have consistently shown maximal activation of the Cpx pathway in bacteria grown to late stationary phase [11,34,84]. Third, maximal rovM expression in Yersinia occurs at late stationary phase when nutrients needed for growth have been exhausted [56,62,64,65]. Where required, antibiotics were added at the final concentrations of carbenicillin (Cb; 100 μg/ml), kanamycin (Km; 50 μg/ml), Trimethoprim (Tp; 10 μg/ml) and chloramphenicol (Cm; 25 μg/ml).…”

“…Control of rovM expression and the CsrA-Crp-RovM-RovA regulatory cascade has clear implications for the lifestyle choices made by Yersinia spp. in terms of planktonic versus sessile growth and survivability in mildly acidic environments or in the flea gut [64][65][66][67].…”