Niche-Specific Impact of a Symbiotic Function on the Persistence of Microbial Symbionts within a Natural Host

Abstract

How the function of microbial symbionts is affected by their population/consortium structure within a host remains poorly understood. The symbiosis established between Euprymna scolopes and Vibrio fischeri is a well-characterized host-microbe association in which the function and structure of V. fischeri populations within the host are known: V. fischeri populations produce bioluminescence from distinct crypt spaces within a dedicated host structure called the light organ. Previous studies have revealed that luminescence is required for V. fischeri populations to persist within the light organ and that deletion of the lux gene locus, which is responsible for luminescence in V. fischeri, leads to a persistence defect. In this study, we investigated the impact of bioluminescence on V. fischeri population structure within the light organ. We report that the persistence defect is specific to crypt I, which is the most developmentally mature crypt space within the nascent light organ. This result provides insight into the structure/function relationship that will be useful for future mechanistic studies of squid-Vibrio symbiosis. In addition, our report highlights the potential impact of the host developmental program on the spatiotemporal dynamics of host-microbe interactions. IMPORTANCEMetazoan development and physiology depend on microbes. The relationship between the symbiotic function of microbes and their spatial structure within the host environment remains poorly understood. Here we demonstrate, using a binary symbiosis, that the host requirement for the symbiotic function of the microbial symbiont is restricted to a specific host environment. Our results also suggest a link between microbial function and host development that may be a fundamental aspect of the more complex host-microbe interactions. Microbes are a dominant form of life on Earth, and their associations with humans and other animals directly impact host development, physiology, and evolution (1-3). In many cases, the acquisition of microbes from the environment represents a key moment in the life history of the host. Studies of mammalian gut microbiota have suggested that the spatial distribution of these microbes within the host, i.e., their biogeography, is an important factor in the assemblage and maintenance of such associations (see reference 4 for a recent review). For instance, when microbial communities isolated from diverse habitats are transplanted into gnotobiotic mice, the resulting composition closely resembles that normally found in the mouse cecum (5). Body part-specific microbiota have also been observed in nonmammalian systems, such as that of the jellyfish Aurelia aurita, which shows significant differences in microbial composition between the gastric cavity and exumbrellar mucus (6). These studies suggest that hosts select certain biogeographical landscapes for their associated microbiota. However, examining how biogeography impacts the symbiotic function of microbes remains challenging for most associations, due in ...

Bacterial Quorum-Sensing Regulation Induces Morphological Change in a Key Host Tissue during the Euprymna scolopes-Vibrio fischeri Symbiosis

“…5C ). Similar to results of earlier studies ( 45 , 46 ), in coinoculations of WT and Δ luxCDABEG strains, the dark mutant was most successful in the less mature crypts, particularly crypt 3 where it was nearly as prevalent as WT ( Fig. 5C ).…”

Progress in and promise of bacterial quorum sensing research

“…Images provided by T. Miyashiro Penn State University. Details of this type of experiment have been published previously 112 .…”

Bacterial symbionts use a type VI secretion system to eliminate competitors in their natural host

“…By labeling two strains with different fluorescent proteins, it is possible to use confocal fluorescence microscopy to identify the strain types of each colonized crypt ( Fig. 7 A – C ) ( 61 , 83 ). For example, in the light organ shown in Fig.…”