Marwa Mamdouh Tawfik, Marlene Lorgen-Ritchie, Elżbieta Król, Stuart McMillan, Fernando Norambuena, Daniel I Bolnick, Alex Douglas, Douglas R Tocher, Mónica B Betancor, Samuel A M Martin
{"title":"大西洋鲑鱼(Salmo salar)通过富含植物的膳食进行营养规划后,肠道微生物群组成和预测代谢能力的变化:对不同发育阶段的认识。","authors":"Marwa Mamdouh Tawfik, Marlene Lorgen-Ritchie, Elżbieta Król, Stuart McMillan, Fernando Norambuena, Daniel I Bolnick, Alex Douglas, Douglas R Tocher, Mónica B Betancor, Samuel A M Martin","doi":"10.1186/s42523-024-00321-8","DOIUrl":null,"url":null,"abstract":"<p><p>To promote sustainable aquaculture, the formulation of Atlantic salmon (Salmo salar) feeds has changed in recent decades, focusing on replacing standard marine-based ingredients with plant-based alternatives, increasingly demonstrating successful outcomes in terms of fish performance. However, little is known about how these plant-based diets may impact the gut microbiota at first feeding and onwards. Nutritional programming (NP) is one strategy applied for exposing fish to a plant-based (V) diet at an early stage in life to promote full utilisation of plant-based ingredients and prevent potential adverse impacts of exposure to a plant-rich diet later in life. We investigated the impact of NP on gut microbiota by introducing fish to plant ingredients (V fish) during first feeding for a brief period of two weeks (stimulus phase) and compared those to fish fed a marine-based diet (M fish). Results demonstrated that V fish not only maintained growth performance at 16 (intermediate phase) and 22 (challenge phase) weeks post first feeding (wpff) when compared to M fish but also modulated gut microbiota. PERMANOVA general effects revealed gut microbiota dissimilarity by fish group (V vs. M fish) and phases (stimulus vs. intermediate vs. challenge). However, no interaction effect of both groups and phases was demonstrated, suggesting a sustained impact of V diet (nutritional history) on fish across time points/phases. Moreover, the V diet exerted a significant cumulative modulatory effect on the Atlantic salmon gut microbiota at 16 wpff that was not demonstrated at two wpff, although both fish groups were fed the M diet at 16 wpff. The nutritional history/dietary regime is the main NP influencing factor, whereas environmental and host factors significantly impacted microbiota composition in M fish. Microbial metabolic reactions of amino acid metabolism were higher in M fish when compared to V fish at two wpff suggesting microbiota played a role in digesting the essential amino acids of M feed. The excessive mucin O-degradation revealed in V fish at two wpff was mitigated in later life stages after NP, suggesting physiological adaptability and tolerance to V diet. 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However, little is known about how these plant-based diets may impact the gut microbiota at first feeding and onwards. Nutritional programming (NP) is one strategy applied for exposing fish to a plant-based (V) diet at an early stage in life to promote full utilisation of plant-based ingredients and prevent potential adverse impacts of exposure to a plant-rich diet later in life. We investigated the impact of NP on gut microbiota by introducing fish to plant ingredients (V fish) during first feeding for a brief period of two weeks (stimulus phase) and compared those to fish fed a marine-based diet (M fish). Results demonstrated that V fish not only maintained growth performance at 16 (intermediate phase) and 22 (challenge phase) weeks post first feeding (wpff) when compared to M fish but also modulated gut microbiota. PERMANOVA general effects revealed gut microbiota dissimilarity by fish group (V vs. M fish) and phases (stimulus vs. intermediate vs. challenge). However, no interaction effect of both groups and phases was demonstrated, suggesting a sustained impact of V diet (nutritional history) on fish across time points/phases. Moreover, the V diet exerted a significant cumulative modulatory effect on the Atlantic salmon gut microbiota at 16 wpff that was not demonstrated at two wpff, although both fish groups were fed the M diet at 16 wpff. The nutritional history/dietary regime is the main NP influencing factor, whereas environmental and host factors significantly impacted microbiota composition in M fish. Microbial metabolic reactions of amino acid metabolism were higher in M fish when compared to V fish at two wpff suggesting microbiota played a role in digesting the essential amino acids of M feed. The excessive mucin O-degradation revealed in V fish at two wpff was mitigated in later life stages after NP, suggesting physiological adaptability and tolerance to V diet. 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引用次数: 0
摘要
为了促进可持续水产养殖,近几十年来大西洋鲑鱼(Salmo salar)饲料的配方发生了变化,重点是用植物性替代品取代标准的海洋性成分,越来越多的替代品在鱼类表现方面取得了成功。然而,人们对这些植物性饲料在首次投喂时及其后可能对肠道微生物群产生的影响知之甚少。营养编程(NP)是一种在鱼类生命早期阶段让其接触植物性(V)膳食的策略,可促进鱼类充分利用植物性成分,并防止鱼类在生命后期接触富含植物的膳食可能产生的不利影响。我们研究了 NP 对肠道微生物群的影响,方法是让鱼类在首次摄食植物配料(V 类鱼)时短暂摄食两周(刺激阶段),并与摄食海洋性食物(M 类鱼)的鱼类进行比较。结果表明,与 M 型鱼相比,V 型鱼不仅在首次投喂后 16 周(中间阶段)和 22 周(挑战阶段)保持了生长性能,而且还调节了肠道微生物群。PERMANOVA 一般效应显示,不同鱼类组(V 鱼与 M 鱼)和不同阶段(刺激阶段与中间阶段与挑战阶段)的肠道微生物群存在差异。然而,两个组别和阶段之间没有交互效应,这表明 V 型饮食(营养史)在不同时间点/阶段对鱼的影响是持续的。此外,V 型饮食在 16 wpff 时对大西洋鲑肠道微生物群产生了显著的累积调节作用,但在 2 wpff 时未显示出这种作用,尽管两组鱼在 16 wpff 时都摄入了 M 型饮食。营养史/饮食制度是主要的 NP 影响因素,而环境和宿主因素则对 M 型鱼的微生物群组成有显著影响。与 V 型鱼相比,M 型鱼在两个月龄时氨基酸代谢的微生物代谢反应更高,这表明微生物群在消化 M 型饲料中的必需氨基酸方面发挥了作用。在 NP 之后的生命后期,V 型鱼在两个 wpff 阶段发现的粘蛋白 O 过度降解现象得到了缓解,这表明鱼类对 V 型饲料具有生理适应性和耐受性。未来的研究需要更全面地探讨微生物群如何在功能上促进净营养过程。
Modulation of gut microbiota composition and predicted metabolic capacity after nutritional programming with a plant-rich diet in Atlantic salmon (Salmo salar): insights across developmental stages.
To promote sustainable aquaculture, the formulation of Atlantic salmon (Salmo salar) feeds has changed in recent decades, focusing on replacing standard marine-based ingredients with plant-based alternatives, increasingly demonstrating successful outcomes in terms of fish performance. However, little is known about how these plant-based diets may impact the gut microbiota at first feeding and onwards. Nutritional programming (NP) is one strategy applied for exposing fish to a plant-based (V) diet at an early stage in life to promote full utilisation of plant-based ingredients and prevent potential adverse impacts of exposure to a plant-rich diet later in life. We investigated the impact of NP on gut microbiota by introducing fish to plant ingredients (V fish) during first feeding for a brief period of two weeks (stimulus phase) and compared those to fish fed a marine-based diet (M fish). Results demonstrated that V fish not only maintained growth performance at 16 (intermediate phase) and 22 (challenge phase) weeks post first feeding (wpff) when compared to M fish but also modulated gut microbiota. PERMANOVA general effects revealed gut microbiota dissimilarity by fish group (V vs. M fish) and phases (stimulus vs. intermediate vs. challenge). However, no interaction effect of both groups and phases was demonstrated, suggesting a sustained impact of V diet (nutritional history) on fish across time points/phases. Moreover, the V diet exerted a significant cumulative modulatory effect on the Atlantic salmon gut microbiota at 16 wpff that was not demonstrated at two wpff, although both fish groups were fed the M diet at 16 wpff. The nutritional history/dietary regime is the main NP influencing factor, whereas environmental and host factors significantly impacted microbiota composition in M fish. Microbial metabolic reactions of amino acid metabolism were higher in M fish when compared to V fish at two wpff suggesting microbiota played a role in digesting the essential amino acids of M feed. The excessive mucin O-degradation revealed in V fish at two wpff was mitigated in later life stages after NP, suggesting physiological adaptability and tolerance to V diet. Future studies are required to explore more fully how the microbiota functionally contributes to the NP.