The Gut of Geographically Disparate Ciona intestinalis Harbors a Core Microbiota

Abstract

It is now widely understood that all animals engage in complex interactions with bacteria (or microbes) throughout their various life stages. This ancient exchange can involve cooperation and has resulted in a wide range of evolved host-microbial interdependencies, including those observed in the gut. Ciona intestinalis, a filter-feeding basal chordate and classic developmental model that can be experimentally manipulated, is being employed to help define these relationships. Ciona larvae are first exposed internally to microbes upon the initiation of feeding in metamorphosed individuals; however, whether or not these microbes subsequently colonize the gut and whether or not Ciona forms relationships with specific bacteria in the gut remains unknown. In this report, we show that the Ciona gut not only is colonized by a complex community of bacteria, but also that samples from three geographically isolated populations reveal striking similarity in abundant operational taxonomic units (OTUs) consistent with the selection of a core community by the gut ecosystem.

Species specificity of symbiosis and secondary metabolism in ascidians

“…These samples were collected at widely different times (different years) and places, and yet they consistently clustered with a similar microbiome across time and space and grouped differently than other species collected at the same locations (Figure 3b). This finding is also consistent with recent reports of ascidian microbiomes, in which some of the same ascidian species we report here were previously examined in other locations Dishaw et al, 2014). Consistently similar bacteria are found across time and space in these studies, in an ascidian host-specific manner.…”

Whole-Genome Sequences of Three Symbiotic Endozoicomonas Strains

“…However, despite the apparent importance of Endozoicomonas spp., it is not clear how they interact with their host. For example, they are the dominant bacteria in seemingly healthy animals (3, 8, 15, 16), although they have been implicated as the causal agent of disease in fish (17). Clarifying the functional capabilities of Endozoicomonas has been challenging because they reside in or on a host organism and can be difficult to culture (6).…”

Immune-directed support of rich microbial communities in the gut has ancient roots

“…Current laboratory investigations (Dishaw et al, unpublished) suggest that Ciona likely maintains a state of balance (i.e., homeostasis) between tolerance and protection through host epithelial–microbe interactions that promote the maintenance of stable, adherent, microbial communities (Dishaw et al, 2014). Ciona TLRs (Sasaki et al, 2009), as well as additional PRRs [e.g., MBL (Skjoedt et al, 2010)], are differentially expressed in unique sections of the gut.…”

“…VCBPs are expressed in distinct regions along the gut at the onset of developmental maturation and as well as at the onset of feeding, and are highly responsive to microbial products (Liberti et al, 2014). Ciona intestinalis from distinct populations have now been shown to harbor a core set of microbiota in the gut (Dishaw et al, 2014) in which adherent communities likely play key functional roles. How the Ciona immune system helps to discriminate among colonizing bacteria and regulate the population of gut symbionts is unclear, given the reduced complexity of its innate immune repertoire.…”

“…This gene reduction can be highly advantageous in defining the first steps in the dialogue by reducing the set of candidate effectors in the system. For example, while Ciona only appears to possess two TLRs (Sasaki et al, 2009), recent experimental observations suggest that the gut is likely discriminating among microbes in a process coupled to immune mediators possessing immunoglobulin domains (Dishaw et al, 2011; Liberti et al, 2014) to selectively maintain a core microbiota (Dishaw et al, 2014) quite possibly in a fashion reminiscent of vertebrate immune inclusion-exclusion (Everett et al, 2004). …”