Regina McGrane, Gwyn A. Beattie

Light may be an important environmental signal for plant-associated bacteria, particularly those that live on leaves. An integrated network of red/far-red- and blue-light-responsive photosensory proteins is known to inhibit swarming motility in the foliar plant pathogen Pseudomonas syringae pv. syringae B728a. Here we elucidated factors in the red/far-red-light-sensing bacteriophytochrome BphP1 signal transduction pathway and report evidence for a role of BphP1 in multiple stages of the Psyringae B728a life cycle. We report that BphP1 signaling involves the downstream regulator Bsi (bacteriophytochrome-regulated swarming inhibitor) and an acyl-homoserine lactone (AHL) signal. Loss of bphP1 or bsi resulted in the early initiation of swarm tendrils during swarming motility, a phenotype that was dependent on red/far-red light and reversed by exogenous AHL, illustrating that the BphP1-Bsi-AHL pathway inhibits the transition from a sessile state to a motile state. Loss of bphP1 or bsi resulted in larger water-soaked lesions induced on bean (Phaseolus vulgaris) pods and enhanced movement from soil and buried plant tissues to seeds, demonstrating that BphP1 and Bsi negatively regulate virulence and bacterial movement through soil to seeds. Moreover, BphP1, but not Bsi, contributed to leaf colonization; loss of bphP1 reduced survival on leaves immediately following inoculation but enhanced the size of the subsequently established populations. Neither Bsi nor Smp, a swarm motility-promoting regulator identified here, affected leaf colonization, indicating that BphP1-mediated contributions to leaf colonization are, at least in part, independent of swarming motility. These results demonstrate that Psyringae B728a red-light sensing involves a multicomponent, branched regulatory pathway that affects several stages of its life cycle.IMPORTANCE Microbes on plants are particularly well positioned to exploit light cues based on the importance of light to plant growth. Photosensory proteins enable organisms to sense light and respond to light, but their roles in the life cycles of plant microbes are poorly understood. This study investigated the cellular components and ecological roles of red/far-red-light sensing in the foliar bacterial pathogen Pseudomonas syringae The study demonstrated that a bacteriophytochrome photosensory protein functions via a multicomponent, branched regulatory pathway that operates primarily through red/far-red-light-mediated inhibition. This pathway negatively regulates the transition from sessile to motile states under conditions conducive to swarming motility. It also negatively regulates virulence on bean pods, movement through soil to seeds, and survival following inoculation on leaves, but it positively contributes to the eventual establishment of leaf-borne populations. These results provide strong evidence that light sensing modulates behaviors at multiple stages in the life cycle of a nonphotosynthetic, plant microbe.