Department of Plant Pathology and Microbiology, Iowa State University, Ames, IA, USA.
mBio. 2013 Jun 11;4(3):e00334-13. doi: 10.1128/mBio.00334-13.
The biological and regulatory roles of photosensory proteins are poorly understood for nonphotosynthetic bacteria. The foliar bacterial pathogen Pseudomonas syringae has three photosensory protein-encoding genes that are predicted to encode the blue-light-sensing LOV (light, oxygen, or voltage) histidine kinase (LOV-HK) and two red/far-red-light-sensing bacteriophytochromes, BphP1 and BphP2. We provide evidence that LOV-HK and BphP1 form an integrated network that regulates swarming motility in response to multiple light wavelengths. The swarming motility of P. syringae B728a deletion mutants indicated that LOV-HK positively regulates swarming motility in response to blue light and BphP1 negatively regulates swarming motility in response to red and far-red light. BphP2 does not detectably regulate swarming motility. The histidine kinase activity of each LOV-HK and BphP1 is required for this regulation based on the loss of complementation upon mutation of residues key to their kinase activity. Surprisingly, mutants lacking both lov and bphP1 were similar in motility to a bphP1 single mutant in blue light, indicating that the loss of bphP1 is epistatic to the loss of lov and also that BphP1 unexpectedly responds to blue light. Moreover, whereas expression of bphP1 did not alter motility under blue light in a bphP1 mutant, it reduced motility in a mutant lacking lov and bphP1, demonstrating that LOV-HK positively regulates motility by suppressing negative regulation by BphP1. These results are the first to show cross talk between the LOV protein and phytochrome signaling pathways in bacteria, and the similarity of this regulatory network to that of photoreceptors in plants suggests a possible common ancestry. IMPORTANCE Photosensory proteins enable organisms to perceive and respond to light. The biological and ecological roles of these proteins in nonphotosynthetic bacteria are largely unknown. This study discovered that a blue-light-sensing LOV (light, oxygen, or voltage) protein and a red/far-red-light-sensing bacteriophytochrome both regulate swarming motility in the foliar pathogen Pseudomonas syringae. These proteins form an integrated signaling network in which the bacteriophytochrome represses swarming motility in response to red, far-red, and blue light, and LOV positively regulates swarming motility by suppressing bacteriophytochrome-mediated blue-light signaling. This is the first example of cross talk between LOV and phytochrome signaling pathways in bacteria, which shows unexpected similarity to photoreceptor signaling in plants.
非光合细菌中，人们对感光蛋白的生物学和调控作用知之甚少。叶部病原菌丁香假单胞菌有三个感光蛋白编码基因，它们被预测编码蓝光感应 LOV（光、氧或电压）组氨酸激酶（LOV-HK）和两个红光/远红光感应细菌视紫红质 BphP1 和 BphP2。我们提供的证据表明，LOV-HK 和 BphP1 形成一个整合的网络，调节对多种光波长的群集运动。丁香假单胞菌 B728a 缺失突变体的群集运动表明，LOV-HK 正向调控蓝光下的群集运动，BphP1 负向调控红光和远红光下的群集运动。BphP2 不能检测到调控群集运动。基于激酶活性关键残基突变导致其激酶活性丧失，LOV-HK 和 BphP1 的组氨酸激酶活性对于这种调控是必需的。令人惊讶的是，lov 和 bphP1 缺失突变体在蓝光下的运动与 bphP1 单突变体相似，这表明 bphP1 的缺失对 lov 的缺失是上位的，而且 BphP1 出人意料地对蓝光做出反应。此外，虽然 bphP1 突变体在蓝光下表达不会改变运动，但在缺乏 lov 和 bphP1 的突变体中，它会降低运动，这表明 LOV-HK 通过抑制 BphP1 的负调控来正向调节运动。这些结果首次表明，细菌中 LOV 蛋白和植物光敏色素信号通路之间存在串扰，并且该调控网络与植物光受体的相似性表明可能存在共同的祖先。
感光蛋白使生物能够感知和响应光。这些蛋白质在非光合细菌中的生物学和生态作用在很大程度上是未知的。本研究发现，蓝光感应 LOV（光、氧或电压）蛋白和红光/远红光感应细菌视紫红质都调节叶部病原菌丁香假单胞菌的群集运动。这些蛋白形成一个整合的信号网络，其中细菌视紫红质抑制对红光、远红光和蓝光的群集运动，而 LOV 通过抑制细菌视紫红质介导的蓝光信号正向调节群集运动。这是细菌中 LOV 和光敏色素信号通路之间首次发生串扰，表明与植物光受体信号存在出人意料的相似性。
