How do microbial communities assemble in the gut of Atlantic cod in response to diet and novel ingredients?

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The global demand for food and protein continues to rise as the world’s population is set to hit 9.7 Billion by 2050. Reducing demands on meat protein and increasing fish consumption is good for our health and potentially more environmentally sustainable. Fish consumption has already eclipsed beef consumption globally. Aquaculture production of fish is a booming industry that could eventually satisfy global fish food demands and reduce our reliance on wild resources. However, for some fish species, such as the Atlantic cod, capture fishing remains the dominant means of production (> 97%). As a result, many cod stocks are in decline. Consequently, the farming of cod could offer a sustainable and reliable means to meet consumer demand for seafood.

Cod farming is promisingly on the tip of a resurgence with recent progress in the Norwegian industry with Norcod AS, which plans on delivering 25,000 tonnes of cod via farming by 2025 — primarily driven by progress in areas such as broodstock development, larval and juvenile husbandry and advances in grow-out techniques. However, knowledge gaps remain regarding fish health and productivity, including; fish growth, sexual maturation and specific diet formulations; which are crucial for farming success [1]. Researchers are increasingly exploring functional aquafeed supplements to bolster fish health and improve sustainable aquaculture production. Such ingredients include prebiotics, probiotics or macroalgae, for example and can greatly influence the immunity and disease challenges in fish and mitigate antimicrobial resistance. In our research collaboration, we wanted to know if we could supplement the diet of juvenile Atlantic cod with seaweeds (macroalgae; egg wrack [Ascophyllum nodosum] or sea lettuce [Ulva rigida]) in a typical farming setting. We were particularly interested in how the gut microbiome would respond to diet supplementation.

Why the gut microbiome?

In humans, the gut microbiome is a critical system (some even argue it should be viewed as an additional organ [2]). Poor health can be linked to an imbalance (dysbiosis) of the gut microbial communities, while good health and immunity are connected to a ‘healthy’ microbiome. Fish gut research is relatively well established, and I agree with Luna et al. (2022) [3] that now is the time to move beyond characterisation studies and into biotechnological innovations. My background is in biotechnology – and in any biotechnology, the aspiration is to ultimately control and manipulate the microbial communities and predict or foresee their response to stimuli or stressors. Control of complex microbiomes like the gut is incredibly challenging. The system contains billions of microbial species that respond to external cues (e.g. pH), internal cues (e.g. cell functions), and host pressures. Moreover, this environment is constantly in flux. Yet, microbial communities in different systems or individuals can shift in unison. For example, we previously observed in a companion paper; that the gut microbiome development in Atlantic cod converged over time irrespective of diet supplementation [4].

We were curious as to what could explain this! How were the gut communities of different fish fed different diet supplements converging over time? Could we unravel the mechanisms behind this shift in microbial community structure?

Would the mechanisms be the same in a small subset of fish that found one of the diets unpalatable and showed lower growth?

Luckily some neat tools to understand the mechanisms that shape microbial communities already exist. These are ecological assembly tools which are implemented through mathematical models. Understanding these mechanisms, I believe, is a crucial first step to predicting and manipulating the fish gut microbiome for better animal health and resistance to pathogens in aquaculture systems. 

Assembly is broadly described as either stochastic (random) or deterministic (non-random). This has been further expanded into the neutral versus niche hypotheses, whereby stochastic and neutral processes are probable events like births, deaths, mutations and ecological drift (which are neutral to species traits) or non-probably events which are determined by species niche or deterministic processes (like species interactions and environmental conditions). In our work, we have used various tools to understand species colonisation, succession and the processes driving the gut microbial dynamics in Atlantic cod.

Schematic diagram showing some of the forces driving microbial communities.

We tested these tools within the following experimental feed trial:

Experimental set-up.

What did we find?

We learned that the mere presence of microbial species in the cod hindgut was via random assembly. But the abundance of common species was driven by deterministic processes. We implemented the ‘competitive lottery model’ to determine how species compete/colonise in space-limited environments and found specific taxa which conformed to this scheme – while others like Photobacterium (a common species in fish gut studies) did not follow this model. Assembly processes were distinct in the supplemented diets, which was more pronounced in the case of the gut communities from fish that showed lower growth with Ascophyllum nodosum supplementation. The hindgut communities, over time, showed reduced functional redundancy (indicating more unique functions). We then implemented an additional method to determine the robustness of the hindgut microbial communities to taxonomic and functional perturbations – peek inside the paper to see what we found!

Summary of our findings.

What implications do our findings have?

This work sheds valuable insights into what ecological processes drive the hindgut microbiome in juvenile Atlantic cod. Yet it but scratches the surface of this exciting area. Further research into defining the variables driving deterministic assembly, particularly throughout the cod life cycle, can offer an avenue to exploit and manipulate the microbiome in a predictable way for increased fish condition and robustness to stress and disease in aquaculture systems. With the advent of novel functional feed supplements from the biotech industries we will need to explore how these additives can benefit farmed fish species like salmon, trout and marine species such as seabass and bream with a view towards producing robust healthy fish for the consumer. Our approach opens the door to a better understanding of these possibilities. 

References:

[1] Puvanendran, V., Mortensen, A., Johansen, L.H., Kettunen, A., Hansen, Ø.J., Henriksen, E. and Heide, M., 2022. Development of cod farming in Norway: Past and current biological and market status and future prospects and directions. Reviews in Aquaculture, 14(1), pp.308-342.

[2] O'Hara, A.M. and Shanahan, F., 2006. The gut flora as a forgotten organ. EMBO reports, 7(7), pp.688-693.

[3] Luna, G.M., Quero, G.M., Kokou, F. and Kormas, K., 2022. Time to integrate biotechnological approaches into fish gut microbiome research. Current Opinion in Biotechnology, 73, pp.121-127.

[4] Keating, C., Bolton-Warberg, M., Hinchcliffe, J., Davies, R., Whelan, S., Wan, A.H.L., Fitzgerald, R.D., Davies, S.J., Ijaz, U.Z. and Smith, C.J., 2021. Temporal changes in the gut microbiota in farmed Atlantic cod (Gadus morhua) outweigh the response to diet supplementation with macroalgae. Animal microbiome, 3(1), pp.1-21.

Ciara Keating

Post Doctoral Research Associate, University of Glasgow