Gut segments outweigh the diet in shaping the intestinal microbiota composition in grass carp Ctenopharyngodon idellus

Wenwen Feng,Wenxiang Li,Ming Li,Shangong Wu,Jing Zhang,Guitang Wang,Hong Zou,Fan Xiong,Ivan Jakovlić

doi:10.1186/s13568-019-0770-0

Abstract

Although dynamics of the complex microbial ecosystem populating the gastrointestinal tract of animals has profound and multifaceted impacts on host’s metabolism and health, it remains unclear whether it is the intrinsic or extrinsic factors that play a more dominant role in mediating the composition of intestinal microbiota. To address this, we studied the impacts of two strikingly different diets on a herbivorous fish, grass carp (Ctenopharyngodon idellus): a high-protein, low-fiber formula feed, and low-protein, high-fiber Sudan grass. After a 16-week feeding trial, microbial profiles of midgut and hindgut segments in both groups were compared. Bacterial composition was significantly different between the midguts of both groups, but not between the hindguts of two groups. Both PerMANOVA and VPA analyses suggested that gut segments explain a higher proportion of variation in intestinal microbiota than diet. Overall, our results suggest that intestinal compartments are a stronger determinant than diet in shaping the intestinal microbiota. Specifically, whereas diet has a strong impact on the composition of microbiota in proximal gut compartments, this impact is much less pronounced distally, which is likely to be a reflection of a limited ability of some microbial taxa to thrive in the anoxic environment in distal segments.

Highlights

Gastrointestinal tract of animals harbors an extremely diverse and complex microbial ecosystem (Li et al 2017; Torok et al 2008; Wu et al 2012; Xiong et al 2017)
To test the hypothesis that diet should outweigh the intestinal segments in shaping the composition of microbial populations in grass carp, we set up a 16-week feeding experiment using two different diets: FF and SG
In the Atlantic cod (Gadusmorhua L.), Gram-positive Brochothrix and Carnobacterium were dominant in the gut of a fish meal diet-fed fish, Psychrobacter dominated in the bioprocessed soy bean meal group, and Carnobacterium, Chryseobacterium and Psychrobacter glacincola dominated in the soy bean meal diet group (Ringø et al 2006)

Summary

Introduction

Gastrointestinal tract of animals harbors an extremely diverse and complex microbial ecosystem (Li et al 2017; Torok et al 2008; Wu et al 2012; Xiong et al 2017). Characterization of the intestinal microbiota and their ecological function is relatively advanced in humans and model mammals (Ley et al 2006; Zhang et al 2012), but less well understood in fish (Wu et al 2012). Intestinal microbiota of fish are believed to be less complex and less numerous than those of terrestrial vertebrates (Miyake et al 2015). Grass carp (Ctenopharyngodon idellus) is a globally distributed herbivorous fish (Feng et al 2009) whose intestinal microbiota has been studied extensively in recent years (Han et al 2010; Tran et al 2017; Wu et al 2012). Recent investigations indicate that the intestinal microbiota of grass carp is likely to play an indispensable role in nutrient (especially polysaccharide) turnover and fermentation of the host (Hao et al 2017b; Wu et al 2015). Maintaining the homeostasis of intestinal microbiota is likely to be essential for health and

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