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Abstract

Temperate phi H20-like phages are repeatedly identified at
geographically distinct areas as free phage particles or as prophages of
the fish pathogen Vibrio anguillarum. We studied mutants of a lysogenic
isolate of V. anguillarum locked in the quorum-sensing regulatory modes
of low (Delta vanT) and high (Delta vanO) cell densities by in-frame
deletion of key regulators of the quorum-sensing pathway. Remarkably, we
find that induction of the H20-like prophage is controlled by the
quorum-sensing state of the host, with an eightfold increase in phage
particles per cell in high-cell-density cultures of the
quorum-sensing-deficient Delta vanT mutant. Comparative studies with
prophage-free strains show that biofilm formation is promoted at low
cell density and that the H20-like prophage stimulates this behavior. In
contrast, the high-cell-density state is associated with reduced
prophage induction, increased proteolytic activity, and repression of
biofilm. The proteolytic activity may dually function to disperse the
biofilm and as a quorum-sensing-mediated antiphage strategy. We
demonstrate an intertwined regulation of phage-host interactions and
biofilm formation, which is orchestrated by host quorum-sensing
signaling, suggesting that increased lysogeny at high cell density is
not solely a strategy for phages to piggy-back the successful bacterial
hosts but is also a host strategy evolved to take control of the
lysis-lysogeny switch to promote host fitness.