Ecological implications of gene regulation by TfoX and TfoY among diverse Vibrio species

Abstract

Summary Bacteria of the genus Vibrio are common members of aquatic environments where they compete with other prokaryotes and defend themselves against grazing predators. A macromolecular protein complex called the type VI secretion system (T6SS) is used for both purposes. Previous research showed that the sole T6SS of the human pathogen V. cholerae is induced by extracellular (chitin) or intracellular (low c‐di‐GMP levels) cues and that these cues lead to distinctive signalling pathways for which the proteins TfoX and TfoY serve as master regulators. In this study, we tested whether the TfoX‐ and TfoY‐mediated regulation of T6SS, concomitantly with natural competence or motility, was conserved in non‐cholera Vibrio species, and if so, how these regulators affected the production of individual T6SSs in double‐armed vibrios. We show that, alongside representative competence genes, TfoX regulates at least one T6SS in all tested Vibrio species. TfoY, on the other hand, fostered motility in all vibrios but had a more versatile T6SS response in that it did not foster T6SS‐mediated killing in all tested vibrios. Collectively, our data provide evidence that the TfoX‐ and TfoY‐mediated signalling pathways are mostly conserved in diverse Vibrio species and important for signal‐specific T6SS induction.

Diversity in natural transformation frequencies and regulation acrossVibriospecies

“…6A). Similar to a previously published comparison, V. parahaemolyticus had a similar transformation frequency to V. cholerae (35). Because expression of both tfoX and qstR were sufficient to increase transformation frequency in DS40M4 in the absence of luxR , we hypothesized that expression of these two transcription factors might increase transformation frequency in other vibrios.…”

“…The only BB120 gene known to be controlled by TfoX that responded with its induction was qstR , suggesting that TfoX might function in BB120 but perhaps at a reduced capability. This is in accordance with the finding that the V. fischeri tfoX is slightly decreased in the ability to cross-activate the qstR of V. cholerae (35). One additional possibility is that there is a regulatory feedback loop that downregulates transcription levels of structural genes in the absence of a functional pilus ( i.e.…”

c-di-GMP inhibits LonA-dependent proteolysis of TfoY in Vibrio cholerae

“…Homologues of TfoY, such as TfoX of V. cholerae, Sxy-1 of Haemophilus influenzae, and Sxy of E. coli are regulators of DNA uptake and natural transformation in their respective organisms [24,[33][34][35][36]. Prior studies have shown that TfoY does not control competency; TfoY is, however, an activator of motility in diverse Vibrio species and frequently controls T6SSdependent killing as well [24,37]. It is important to note that the stability of Sxy of E. coli is also dependent upon LonA, which suggests that LonA proteolysis of TfoX-like domain containing proteins may be a common regulatory mechanism in diverse bacterial species [33].…”

“…coli are regulators of DNA uptake and natural transformation in their respective organisms [ 24 , 33 – 36 ]. Prior studies have shown that TfoY does not control competency; TfoY is, however, an activator of motility in diverse Vibrio species and frequently controls T6SS-dependent killing as well [ 24 , 37 ]. It is important to note that the stability of Sxy of E .…”

“…While the environmental signals that govern the production of TfoY remain unclear, it has become increasingly apparent that sustained sensing of c-di-GMP by multiple c-di-GMP receptors is critical in controlling TfoY synthesis and turnover ( Fig 7 ) [ 24 , 26 , 27 , 37 , 41 – 43 ]. For example, TfoY is regulated at the transcriptional level via a c-di-GMP binding transcriptional factor; at the post-transcriptional level via a c-di-GMP dependent riboswitch; and at the post-translational level via c-di-GMP modulated proteolysis.…”