Interactions of Symbiotic Partners Drive the Development of a Complex Biogeography in the Squid-Vibrio Symbiosis

Interactions of Symbiotic Partners Drive the Development of a Complex Biogeography in the Squid-Vibrio Symbiosis
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DOI:
10.1128/mbio.00853-20
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发表时间:
2020-05-01
期刊:
影响因子:
6.4
通讯作者:
McFall-Ngai, Margaret J.
McFall-Ngai, Margaret J.
中科院分区:
生物学1区
文献类型:
--
作者:
Essock-Burns, Tara;Bongrand, Clotilde;McFall-Ngai, Margaret J.

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微生物生活在宿主组织内复杂的微生态位中,但共生伙伴如何在发育过程中沟通以创造这样的微生态位,在很大程度上尚未探索。使用共聚焦显微镜和共生体遗传学,我们的特点是塑造的主机微环境在光器官殖民化的鱿鱼Euprymna speopes由细菌弧菌fischeri。在胚胎发生过程中,三对内陷依次形成在器官的表面,产生孔,导致内部压缩小管在不同的发展阶段。孵化后,这些区域扩大,允许V.fischeri细胞进入并通过三个解剖学上不同的区域迁移120 μ m,然后到达盲端隐窝空间。一个动态的看门人或瓶颈将这些隐窝与迁移路径连接起来。一旦费氏弧菌细胞进入隐窝,瓶颈就会变窄,共生体种群的定殖在空间上受到限制。缩窄和限制的实际时间随隐窝成熟度和不同的费氏弧菌菌株而变化。随后,从殖民化后的第一个黎明开始,瓶颈控制着黎明触发的大多数共生体驱逐到环境中的终身循环,以及随后在地穴中的再生长。与其他发育表型不同,瓶颈收缩不是由已知的微生物相关分子模式(MAMP)或费氏弧菌产生的生物发光诱导的,但它确实需要代谢活性共生体。此外,虽然最成熟的隐窝中的共生体具有更高比例的活细胞,并且在黎明时排出的可能性更大,但它们对抗生素的抗性较低。这些不同的微环境的整体动态反映了主机共生dialogue.IMPORTANCE的复杂性,不可访问性,和大多数动物微生物的初始定植的时间尺度的复杂性,提出了挑战的表征细菌共生体如何影响组织的形式和功能,在几分钟到几个小时后,最初的相互作用的合作伙伴。在这里,我们使用自然发生的二进制鱿鱼弧菌协会来探索这一现象。这种共生的时空景观在其发病过程中的成像提供了一个窗口,在宿主组织成熟和共生菌株表型的差异对建立一个动态稳定的共生系统的影响。这些数据提供的证据表明,共生体形状的宿主组织景观和组织成熟的影响菌株水平差异的影响,每日的共生节奏,殖民化的竞争力,和抗生素敏感性。
Microbes live in complex microniches within host tissues, but how symbiotic partners communicate to create such niches during development remains largely unexplored. Using confocal microscopy and symbiont genetics, we characterized the shaping of host microenvironments during light organ colonization of the squid Euprymna scolopes by the bacterium Vibrio fischeri. During embryogenesis, three pairs of invaginations form sequentially on the organ's surface, producing pores that lead to interior compressed tubules at different stages of development. After hatching, these areas expand, allowing V. fischeri cells to enter and migrate similar to 120 mu m through three anatomically distinct regions before reaching blind-ended crypt spaces. A dynamic gatekeeper, or bottleneck, connects these crypts with the migration path. Once V. fischeri cells have entered the crypts, the bottlenecks narrow, and colonization by the symbiont population becomes spatially restricted. The actual timing of constriction and restriction varies with crypt maturity and with different V. fischeri strains. Subsequently, starting with the first dawn following colonization, the bottleneck controls a lifelong cycle of dawn-triggered expulsions of most of the symbionts into the environment and a subsequent regrowth in the crypts. Unlike other developmental phenotypes, bottleneck constriction is not induced by known microbe-associated molecular patterns (MAMPs) or by V. fischeri-produced bioluminescence, but it does require metabolically active symbionts. Further, while symbionts in the most mature crypts have a higher proportion of live cells and a greater likelihood of expulsion at dawn, they have a lower resistance to antibiotics. The overall dynamics of these distinct microenvironments reflect the complexity of the host-symbiont dialogue.IMPORTANCE The complexity, inaccessibility, and time scales of initial colonization of most animal microbiomes present challenges for the characterization of how the bacterial symbionts influence the form and function of tissues in the minutes to hours following the initial interaction of the partners. Here, we use the naturally occurring binary squid-vibrio association to explore this phenomenon. Imaging of the spatiotemporal landscape of this symbiosis during its onset provides a window into the impact of differences in both host-tissue maturation and symbiont strain phenotypes on the establishment of a dynamically stable symbiotic system. These data provide evidence that the symbionts shape the host-tissue landscape and that tissue maturation impacts the influence of strain-level differences on the daily rhythms of the symbiosis, the competitiveness for colonization, and antibiotic sensitivity.