The high-pathogenicity island
irp
-HPI is widespread in
Vibrionaceae
and encodes the siderophore piscibactin, as well as the regulator PbtA that is essential for its expression. In this work, we aim to study whether PbtA directly interacts with
irp
-HPI promoters. Furthermore, we hypothesize that PbtA, and thereby the acquisition of
irp
-HPI island, may also influence the expression of other genes elsewhere in the bacterial genome. To address this question, an RNAseq analysis was conducted to identify differentially expressed genes after
pbtA
deletion in
Vibrio anguillarum
RV22 genetic background. The results showed that PbtA not only modulates the
irp
-HPI genes but also modulates the expression of a plethora of
V. anguillarum
core genome genes, inducing nitrate, arginine, and sulfate metabolism, T6SS1, and quorum sensing, while repressing lipopolysaccharide (LPS) production, MARTX toxin, and major porins such as OmpV and ChiP. The direct binding of the C-terminal domain of PbtA to piscibactin promoters (P
frpA
and P
frpC
), quorum sensing (
vanT
), LPS transporter
wza,
and T6SS structure- and effector-encoding genes was demonstrated by electrophoretic mobility shift assay (EMSA). The results provide valuable insights into the regulatory mechanisms underlying the expression of
irp
-HPI island and its impact on Vibrios transcriptome, with implications in pathogenesis.
IMPORTANCE
Horizontal gene transfer enables bacteria to acquire traits, such as virulence factors, thereby increasing the risk of the emergence of new pathogens.
irp
-HPI genomic island has a broad dissemination in
Vibrionaceae
and is present in numerous potentially pathogenic marine bacteria, some of which can infect humans. Previous works showed that certain
V. anguillarum
strains exhibit an expanded host range plasticity and heightened virulence, a phenomenon linked to the acquisition of the
irp
-HPI genomic island. The present work shows that this adaptive capability is likely achieved through comprehensive changes in the transcriptome of the bacteria and that these changes are mediated by the master regulator PbtA encoded within the
irp
-HPI element. Our results shed light on the broad implications of horizontal gene transfer in bacterial evolution, showing that the acquired DNA can directly mediate changes in the expression of the core genome, with profounds implications in pathogenesis.