Gundlach Katrina A, Nawroth Janna, Kanso Eva, Nasrin Farzana, Ruby Edward G, McFall-Ngai Margaret
Kewalo Marine Laboratory, University of Hawai'i at Mānoa, Honolulu, HI, United States.
Helmholtz Pioneer Campus, Helmholtz Zentrum München, Neuherberg, Germany.
Front Cell Dev Biol. 2022 Oct 20;10:974213. doi: 10.3389/fcell.2022.974213. eCollection 2022.
The Hawaiian bobtail squid, , harvests its luminous symbiont, , from the surrounding seawater within hours of hatching. During embryogenesis, the host animal develops a nascent light organ with ciliated fields on each lateral surface. We hypothesized that these fields function to increase the efficiency of symbiont colonization of host tissues. Within minutes of hatching from the egg, the host's ciliated fields shed copious amounts of mucus in a non-specific response to bacterial surface molecules, specifically peptidoglycan (PGN), from the bacterioplankton in the surrounding seawater. Experimental manipulation of the system provided evidence that nitric oxide in the mucus drives an increase in ciliary beat frequency (CBF), and exposure to even small numbers of cells for short periods resulted in an additional increase in CBF. These results indicate that the light-organ ciliated fields respond specifically, sensitively, and rapidly, to the presence of nonspecific PGN as well as symbiont cells in the ambient seawater. Notably, the study provides the first evidence that this induction of an increase in CBF occurs as part of a thus far undiscovered initial phase in colonization of the squid host by its symbiont, i.e., host recognition of cues in the environment within minutes. Using a biophysics-based mathematical analysis, we showed that this rapid induction of increased CBF, while accelerating bacterial advection, is unlikely to be signaled by cells interacting directly with the organ surface. These overall changes in CBF were shown to significantly impact the efficiency of colonization of the host organ. Further, once has fully colonized the host tissues, i.e., about 12-24 h after initial host-symbiont interactions, the symbionts drove an attenuation of mucus shedding from the ciliated fields, concomitant with an attenuation of the CBF. Taken together, these findings offer a window into the very first interactions of ciliated surfaces with their coevolved microbial partners.
夏威夷短尾乌贼在孵化后的数小时内,就从周围海水中获取其发光共生体。在胚胎发育过程中,宿主动物会发育出一个新生的发光器官,其每个侧面都有纤毛区域。我们推测这些区域的功能是提高共生体在宿主组织中定殖的效率。从卵中孵化出来后的几分钟内,宿主的纤毛区域会因对周围海水中浮游细菌表面分子(特别是肽聚糖,PGN)的非特异性反应而分泌大量黏液。对该系统的实验操作提供了证据,表明黏液中的一氧化氮会促使纤毛摆动频率(CBF)增加,并且即使短时间暴露于少量细胞也会导致CBF进一步增加。这些结果表明,发光器官的纤毛区域对环境海水中非特异性PGN以及共生体细胞的存在具有特异性、敏感性和快速的反应。值得注意的是,该研究首次提供了证据,表明CBF增加的这种诱导是乌贼宿主被其共生体定殖的一个迄今未被发现的初始阶段的一部分,即在几分钟内宿主对环境中的线索进行识别。通过基于生物物理学的数学分析,我们表明CBF的这种快速增加虽然加速了细菌平流,但不太可能是由细胞与器官表面直接相互作用发出的信号。CBF的这些总体变化被证明会显著影响宿主器官的定殖效率。此外,一旦完全定殖于宿主组织,即初始宿主 - 共生体相互作用后约12 - 24小时,共生体会促使纤毛区域黏液分泌减少,同时CBF也会减弱。综上所述,这些发现为纤毛表面与其共同进化的微生物伙伴之间的首次相互作用提供了一个窗口。