Research & Development, Emulate Inc., Boston, MA 02210.
Graduate Aeronautical Laboratories and Bioengineering, California Institute of Technology, Pasadena, CA 91125.
Proc Natl Acad Sci U S A. 2017 Sep 5;114(36):9510-9516. doi: 10.1073/pnas.1706926114. Epub 2017 Aug 23.
We show that mucociliary membranes of animal epithelia can create fluid-mechanical microenvironments for the active recruitment of the specific microbiome of the host. In terrestrial vertebrates, these tissues are typically colonized by complex consortia and are inaccessible to observation. Such tissues can be directly examined in aquatic animals, providing valuable opportunities for the analysis of mucociliary activity in relation to bacteria recruitment. Using the squid-vibrio model system, we provide a characterization of the initial engagement of microbial symbionts along ciliated tissues. Specifically, we developed an empirical and theoretical framework to conduct a census of ciliated cell types, create structural maps, and resolve the spatiotemporal flow dynamics. Our multiscale analyses revealed two distinct, highly organized populations of cilia on the host tissues. An array of long cilia ([Formula: see text]25 [Formula: see text]m) with metachronal beat creates a flow that focuses bacteria-sized particles, at the exclusion of larger particles, into sheltered zones; there, a field of randomly beating short cilia ([Formula: see text]10 [Formula: see text]m) mixes the local fluid environment, which contains host biochemical signals known to prime symbionts for colonization. This cilia-mediated process represents a previously unrecognized mechanism for symbiont recruitment. Each mucociliary surface that recruits a microbiome such as the case described here is likely to have system-specific features. However, all mucociliary surfaces are subject to the same physical and biological constraints that are imposed by the fluid environment and the evolutionary conserved structure of cilia. As such, our study promises to provide insight into universal mechanisms that drive the recruitment of symbiotic partners.
我们证明,动物上皮的黏液纤毛膜可以为宿主的特定微生物组的主动募集创造流体力学微环境。在陆生脊椎动物中,这些组织通常被复杂的共生体定植,并且无法观察到。在水生动物中,可以直接检查这些组织,为分析与细菌募集相关的黏液纤毛活性提供了有价值的机会。使用鱿鱼-弧菌模型系统,我们对微生物共生体沿着纤毛组织的初始结合进行了特征描述。具体来说,我们开发了一个经验和理论框架,对纤毛细胞类型进行普查,创建结构图谱,并解析时空流动动力学。我们的多尺度分析揭示了宿主组织上两种截然不同的、高度组织化的纤毛群体。一排长纤毛([Formula: see text]25 [Formula: see text]m)以同步跳动产生的流动将细菌大小的颗粒聚焦在遮蔽区域内,而排除了更大的颗粒;在那里,随机跳动的短纤毛([Formula: see text]10 [Formula: see text]m)的场混合了局部流体环境,其中包含已知可使共生体定植的宿主生化信号。这种纤毛介导的过程代表了一种以前未被识别的共生体募集机制。像这里描述的那样,招募微生物组的每个黏液纤毛表面都可能具有系统特异性特征。然而,所有的黏液纤毛表面都受到流体环境和纤毛的进化保守结构所施加的相同物理和生物学限制的制约。因此,我们的研究有望为驱动共生伙伴招募的普遍机制提供深入了解。