The impact of nutritional programming on the microbiota of different gut regions in Atlantic Salmon (Salmo salar) from first feeding in a 22-week feeding trial

Author:

Tawfik Marwa Mamdouh1,Tocher Douglas R.2,McMillan Stuart2,Norambuena Fernando3,Douglas Alex1,Betancor Mónica B.2,Martin Samuel A. M.1

Affiliation:

1. University of Aberdeen

2. University of Stirling

3. BioMar (United Kingdom)

Abstract

Abstract

Increasing evidence suggests that gut microbiota is essential for regulating the development of the digestive system, aiding digestion, nutrient metabolism, growth, immune function, and disease resistance. Advances in high throughput sequencing technologies have allowed the development of a broader understanding of the complex gut microbiota in fish, especially in relation to the impact of dietary plant ingredients on gut health. However, to date, most studies have focused on the entire or distal gut in response to a plant-based diet. Moreover, the potential involvement of the microbiome in driving the adaptation of early-exposed Atlantic salmon to a plant-based diet during a later developmental stage, a phenomenon commonly referred to as ‘nutritional programming’, has yet to be demonstrated. The aim was to characterise and compare the microbiota composition and diversity in gut regions (pyloric caeca, middle and distal intestines) of Atlantic salmon (maintained for 22 weeks from first feeding in a recirculating aquaculture system) with and without nutritional programming using a plant-based diet. 16S rRNA amplicons sequencing was employed to monitor taxa and were identified as amplicon sequence variants. The study experiment followed a typical nutritional programming design with two experimental groups. Fish initially exposed to the plant-based diet for two weeks at first feeding and challenged later at 16 weeks post first-feeding for six weeks with a similar plant-based diet were considered the programmed group, whereas those initially fed a marine diet and challenged later with the plant-based diet were the control group. The alpha diversity was higher in the pyloric caeca than the distal intestine. Analysis of similarities showed that the microbiota of pyloric caeca differentiated in composition from each of middle and distal regions after nutritional programming in both high and low-abundant taxa. Ruminococcaceae (primarily anaerobic Clostridia) comprised the core taxa in 80% of fish in the programmed group across the three gut regions and is known to help ferment plant ingredients. Moreover, the internal environment of each gut region mainly selects their microbial assemblages. Additionally, sequencing of feed and water revealed their influence on the gut microbiota of programmed and control fish. Furthermore, Firmicutes, Proteobacteria, Actinobacteriota and Bacteroidota were the prevalent and dominant phyla regardless of the gut region. Further research is required to better understand the microbial programming and its functional consequences in carnivorous fish.

Publisher

Springer Science and Business Media LLC

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