Pacific Biosciences Research Center, University of Hawai'i at Mānoa, Honolulu, Hawai'i, USA.
mBio. 2021 Oct 26;12(5):e0240221. doi: 10.1128/mBio.02402-21. Epub 2021 Sep 28.
Microbes colonize the apical surfaces of polarized epithelia in nearly all animal taxa. In one example, the luminous bacterium Vibrio fischeri enters, grows to a dense population within, and persists for months inside, the light-emitting organ of the squid Euprymna scolopes. Crucial to the symbiont's success after entry is the ability to trigger the constriction of a host tissue region (the "bottleneck") at the entrance to the colonization site. Bottleneck constriction begins at about the same time as bioluminescence, which is induced in V. fischeri through an autoinduction process called quorum sensing. Here, we asked the following questions: (i) Are the quorum signals that induce symbiont bioluminescence also involved in triggering the constriction? (ii) Does improper signaling of constriction affect the normal maintenance of the symbiont population? We manipulated the presence of three factors, the two V. fischeri quorum signal synthases, AinS and LuxI, the transcriptional regulator LuxR, and light emission itself, and found that the major factor triggering and maintaining bottleneck constriction is an as yet unknown effector(s) regulated by LuxIR. Treating the animal with chemical inhibitors of actin polymerization reopened the bottlenecks, recapitulating the host's response to quorum-sensing defective symbionts, as well as suggesting that actin polymerization is the primary mechanism underlying constriction. Finally, we found that these host responses to the presence of symbionts changed as a function of tissue maturation. Taken together, this work broadens our concept of how quorum sensing can regulate host development, thereby allowing bacteria to maintain long-term tissue associations. Interbacterial signaling within a host-associated population can have profound effects on the behavior of the bacteria, for instance, in their production of virulence/colonization factors; in addition, such signaling can dictate the nature of the outcome for the host, in both pathogenic and beneficial associations. Using the monospecific squid-vibrio model of symbiosis, we examined how quorum-sensing regulation by the Vibrio fischeri population induces a biogeographic tissue phenotype that promotes the retention of this extracellular symbiont within the light organ of its host, Euprymna scolopes. Understanding the influence of bacterial symbionts on key sites of tissue architecture has implications for all horizontally transmitted symbioses, especially those that colonize an epithelial surface within the host.
微生物在几乎所有动物类群的极化上皮的顶端表面定植。在一个例子中，发光细菌 Vibrio fischeri 进入，在鱿鱼 Euprymna scolopes 的发光器官内生长到密集的种群，并持续数月。共生体进入后的成功关键是能够触发定植部位入口处的宿主组织区域（“瓶颈”）收缩。瓶颈收缩大约与生物发光同时开始，生物发光通过称为群体感应的自动感应过程在 V. fischeri 中诱导。在这里，我们提出了以下问题：（i）诱导共生体生物发光的群体信号是否也参与触发收缩？（ii）收缩信号的不当传递是否会影响共生体种群的正常维持？我们操纵了三种因素的存在，即两个 Vibrio fischeri 群体信号合酶 AinS 和 LuxI、转录调节剂 LuxR 和光发射本身，并发现触发和维持瓶颈收缩的主要因素是一个尚未知的效应物（s），受 LuxIR 调节。用肌动蛋白聚合的化学抑制剂处理动物，重新打开瓶颈，再现了宿主对群体感应缺陷共生体的反应，这也表明肌动蛋白聚合是收缩的主要机制。最后，我们发现，宿主对共生体存在的这些反应随着组织成熟而变化。总之，这项工作拓宽了我们对群体感应如何调节宿主发育的概念，从而使细菌能够维持长期的组织联系。 宿主相关群体内的细菌间信号传递可以对细菌的行为产生深远影响，例如，在其产生毒力/定植因子方面；此外，这种信号传递可以决定宿主的结果性质，无论是在致病性还是有益性的关联中。使用 Vibrio fischeri 群体的单特异性鱿鱼- vibrio 共生模型，我们研究了群体感应调节如何诱导生物地理组织表型，从而促进这种细胞外共生体在其宿主 Euprymna scolopes 的发光器官内的保留。了解细菌共生体对组织架构关键部位的影响对于所有水平传播的共生关系都具有重要意义，特别是那些在宿主内定植上皮表面的共生关系。
