The role of the gut microbiome in sustainable teleost aquaculture

Abstract

As the most diverse vertebrate group and a major component of a growing global aquaculture industry, teleosts continue to attract significant scientific attention. The growth in global aquaculture, driven by declines in wild stocks, has provided additional empirical demand, and thus opportunities, to explore teleost diversity. Among key developments is the recent growth in microbiome exploration, facilitated by advances in high-throughput sequencing technologies. Here, we consider studies on teleost gut microbiomes in the context of sustainable aquaculture, which we have discussed in four themes: diet, immunity, artificial selection and closed-loop systems. We demonstrate the influence aquaculture has had on gut microbiome research, while also providing a road map for the main deterministic forces that influence the gut microbiome, with topical applications to aquaculture. Functional significance is considered within an aquaculture context with reference to impacts on nutrition and immunity. Finally, we identify key knowledge gaps, both methodological and conceptual, and propose promising applications of gut microbiome manipulation to aquaculture, and future priorities in microbiome research. These include insect-based feeds, vaccination, mechanism of pro- and prebiotics, artificial selection on the hologenome, in-water bacteriophages in recirculating aquaculture systems (RAS), physiochemical properties of water and dysbiosis as a biomarker.

Keywords: aquaculture; fish; gut; microbiome; review; teleost.

Figure 1.

(a) Number of studies on the gut microbiome using NGS broken down by the genus of fish that the study was conducted on, as well as the environment those fish same from. Asterisk represents salmonid, carp and talapia. (b) The number of studies that assessed the water microbial communities. Gut microbiome studies were compiled using Web of Science [4] and only include studies that implemented NGS. It is acknowledged that total microbiome research extends further than this. Further information on search terms and filtering can be found in the electronic supplementary material. (Online version in colour.)

Figure 2.

Growth in the studies using NGS on fish gut microbiomes, including food aquaculture species (aquaculture status taken from FishBase [12]). Further information on search terms and filtering can be found in the electronic supplementary material. (Online version in colour.)

Figure 3.

(a) Schematic view of the deterministic processes that influence gut microbial communities in fish. Community assemblage of bacteria in the gut starts with inputs from the environment (green), such as the bacteria within the water column, or in solid particulates of biofilm, sediment and feed. Once ingested, these bacteria are influenced by interacting deterministic processes (brown) such as the host's abiotic gut environment, interaction with the hosts' physiology through the gut lining and its secretions, as well as interactions between other microbiomes. The outcome (red) is final community assembly, which can be characterized using an array of cutting-edge molecular techniques (purple). A subset of the boarder interactions is provided, with focus on (b) microbe–environment–host interactions, (c) host gut physiology and (d) behaviour. (Online version in colour.)

Figure 4.

Schematic diagram of (a) feed inputs (green), (b) water processing (both RAS and BFT) (blue) and the (c) species being cultivated, along with its gut microbiome (red). (Online version in colour.)

Figure 5.

Methodological approaches used in high-throughput sequencing of fish gut microbiomes, broken down by the type of sequencing platform and genetic marker. Marker types are predominantly variable regions (V) within the 16S ribosomal RNA gene. Further information on search terms and filtering can be found in the electronic supplementary material. (Online version in colour.)