Teleost microbiomes: the state of the art in their characterization, manipulation and importance in aquaculture and fisheries

Abstract

Indigenous microbiota play a critical role in the lives of their vertebrate hosts. In human and mouse models it is increasingly clear that innate and adaptive immunity develop in close concert with the commensal microbiome. Furthermore, several aspects of digestion and nutrient metabolism are governed by intestinal microbiota. Research on teleosts has responded relatively slowly to the introduction of massively parallel sequencing procedures in microbiomics. Nonetheless, progress has been made in biotic and gnotobiotic zebrafish models, defining a core microbiome and describing its role in development. However, microbiome research in other teleost species, especially those important from an aquaculture perspective, has been relatively slow. In this review, we examine progress in teleost microbiome research to date. We discuss teleost microbiomes in health and disease, microbiome ontogeny, prospects for successful microbiome manipulation (especially in an aquaculture setting) and attempt to identify important future research themes. We predict an explosion in research in this sector in line with the increasing global demand for fish protein, and the need to find sustainable approaches to improve aquaculture yield. The reduced cost and increasing ease of next generation sequencing technologies provides the technological backing, and the next 10 years will be an exciting time for teleost microbiome research.

Keywords: aquaculture; fish; fisheries; microbiota; probiotics.

Figure 1

General microbiological findings on fish microbiota. This overview synthesizes the major phyla present in the different organs of fish from different species. Bacterial phyla included are correspond to those which made up >80% of sequences characterized from a given tissue/organ in each study. Only studies that employed direct sequencing (clone libraries/amplico-seq) are included.

Figure 2

Host microbiota interactions during homeostasis and dysbiosis. The host is able to control the pathogen (c) growth by different process (A,C) involving the immune response (a) and the resident microbiota (b). Furthermore, the immune response recognizes the resident microbiota (D) as non-pathogenic bacteria. Pathogenic bacteria auto-regulate abundance via quorum sensing (B) and can detect environmental signals from host cells [epidermic cells (d) and mucous cells (e)]. During dysbiosis, the pathogenic population, triggered by the stress response of the host (diminution of the immune response, production of mucus and diminution of the abundance of the resident microbiota), overcome the immune response and outcompete the resident microbiota.

Figure 3

Teleost microbiome during development. Figure shows schematic of the generalized lifecycle of a teleost and accessory indigenous bacteria (different taxa represented by colored elipses). (1) Bacteria colonize the chorion of the egg. Taxonomic differences of bacteria between fish species suggest specific early interactions, perhaps through precursors of innate immunity (symbolized by squares and triangles on the chorion surface). (2) Egg hatches, larval is colonized by environmental bacteria as well as those originally present on the chorion. (3) Early digestive tract colonization occurs when larva commence feeding. Bacterial taxa strongly resemble those associated with food source. (4) Microbiome develops, accumulates diversity and matures. (5) Adult microbiome is diverse assemblage of microbial taxa. Differences exist between surface mucosal and intestinal communities. Intestinal communities also be compartmentalized/specialized to niches within the alimentary tract. Question mark indicates possible vertical transmission of microbiome components to eggs during oviposition.