Abstract
The functional ecology of the gastrointestinal tract impacts host physiology, and its dysregulation is at the center of various diseases. The immune system, and specifically innate immunity, plays a fundamental role in modulating the interface of host and microbes in the gut. While humans remain a primary focus of research in this field, the use of diverse model systems help inform us of the fundamental principles legislating homeostasis in the gut. Invertebrates, which lack vertebrate-style adaptive immunity, can help define conserved features of innate immunity that shape the gut ecosystem. In this context, we previously proposed the use of a marine invertebrate, the protochordate Ciona robusta, as a novel tractable model system for studies of host-microbiome interactions. Significant progress, reviewed herein, has been made to fulfill that vision. We examine and review discoveries from Ciona that include roles for a secreted immune effector interacting with elements of the microbiota, as well as chitin-rich mucus lining the gut epithelium, the gut-associated microbiome of adults, and the establishment of a large catalog of cultured isolates with which juveniles can be colonized. Also discussed is the establishment of methods to rear the animals germ-free, an essential technology for dissecting the symbiotic interactions at play. As the foundation is now set to extend these studies into the future, broadening our comprehension of how host effectors shape the ecology of these microbial communities in ways that establish and maintain homeostasis will require full utilization of “multi-omics” approaches to merge computational sciences, modeling, and experimental biology in hypothesis-driven investigations.
Highlights
The gut environment includes a dynamic community of microorganisms, consisting mainly of bacteria, and Archaea, viruses, fungi, protozoans, and occasionally, helminthic worms
The modern realization that complex animal-associated microbial communities most often serve as vital symbiotic interactions or evolved interdependencies shaping physiology and homeostasis has resulted in an urgent need for studying diverse model systems
We focus our attention on the invertebrate chordate model Ciona robusta, first proposed by Dishaw et al in 2012 as a novel tractable model system for studies of host-microbial interactions within the gut [18], and review the important advancements made far
Summary
The gut environment includes a dynamic community of microorganisms, consisting mainly of bacteria, and Archaea, viruses, fungi, protozoans, and occasionally, helminthic worms. We will recapitulate recent efforts to characterize the Ciona gut environment, including the presence of a gut epithelium layered with chitin-rich mucus and roles for a secreted immune effector family, namely the immunoglobulin (Ig)-like variable region-containing chitin-binding proteins (VCBPs), interacting with distinct elements of the microbiome. The use of multi-omics approaches in Ciona, as well as in other organisms, may enable a more holistic view of microbiome composition and function at multiple layers [141, 149], facilitating hypothesis-driven experimentation to ascertain mechanisms of homeostasis and help define roles for immune effectors, and their interactions with specific components of these complex microbial communities. Future drug discovery efforts depend on harnessing powerful new technologies and model systems, while integrating information from sequenced genomes, functional genomics, protein profiling, metabolomics, and bioinformatics, in a manner that ensures a comprehensive systems-based analysis that furthers our understanding of the complexities of health and disease [167, 168]
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