Fucoidan Improves Growth, Digestive Tract Maturation, and Gut Microbiota in Large Yellow Croaker (Larimichthys crocea) Larvae

Abstract

The early life period is considered an essential period for gut microbial colonization. Manipulating gut microbiota interventions during early life periods has been proven to be a promising method to boost healthy growth. Therefore, the aim of the present study was to investigate the effects of dietary fucoidan (Fuc) on the growth, digestive tract maturation, and gut microbiota of large yellow croaker (Larimichthys crocea) larvae. Four diets were formulated with different levels of Fuc (0.00%, 0.50%, 1.00%, and 2.00%). Results showed that dietary Fuc significantly improved the growth performance of larvae. Meanwhile, dietary Fuc promoted digestive tract maturation. Dietary 1.00% Fuc significantly improved intestinal morphology. Dietary Fuc upregulated the expression of intestinal cell proliferation and differentiation related-genes and intestinal barrier related-genes. Dietary 2.00% Fuc significantly increased the activities of brush border membranes enzymes and lipase while inhibiting α-amylase. Furthermore, dietary Fuc maintained healthy intestinal micro-ecology. In detail, dietary 1.00% and 2.00% Fuc altered the overall structure of the gut microbiota and increased the relative abundance of Bacteroidetes while decreasing the relative abundance of opportunistic pathogens and facultative anaerobe. In conclusion, appropriate dietary Fuc (1.00-2.00%) could improve the growth of large yellow croaker larvae by promoting digestive tract maturation and maintaining an ideal intestinal micro-ecology.

Keywords: digestive tract maturation; early life intervention; fucoidan; gut microbiota; large yellow croaker larvae.

Figure 1

Flow graph of experimental procedure and design (DAH: days after hatch; IS: intestinal segments; PS: pancreatic segments).

Figure 2

Effects of dietary fucoidan on intestinal cell proliferation and differentiation-related genes mRNA expression (a) and intestinal barrier-related genes mRNA expression (b) in the intestinal tract of large yellow croaker larvae. Values are means (n = 3), with their standard errors represented by vertical bars. Bars bearing the same letters were not significantly different (p > 0.05, Tukey’s test).

Figure 3

Effects of dietary fucoidan on gut microbial structure of large yellow croaker larvae (n = 3/group). (a) Venn diagram; (b) principal component analysis (PCA); (c) unweighted uniFrac distance matrix.

Figure 4

Effects of dietary fucoidan on gut microbial composition of large yellow croaker larvae (n = 3/group). (a–c) Taxonomy classification of reads at phylum (a), genus (b) and specie (c) taxonomic levels. Only the top 10 most abundant (Based on relative abundance) bacterial phyla, genera and species were shown in the figures. Other phyla, genera and species were all assigned as ‘Others’. (d,e) LefSe analysis identified the most differentially abundant taxons among the Fuc0, Fuc0.5, Fuc1, and Fuc2 groups.

Figure 5

Effects of dietary fucoidan on oxygen utilization of microbial community of large yellow croaker larvae based on BugBase analysis. (a) Facultatively anaerobic bacteria; (b) anaerobic bacteria; (c) aerobic bacteria. The outcome was grouped according the modules (x-axis). The relative abundance is presented on the y-axis. Pairwise Mann–Whitney–Wilcoxon tests were performed for data analysis between the Fuc0 group and other Fuc groups (*, p < 0.05).

Figure 6

Effects of dietary fucoidan on the relative abundance of gut microbiota that correlated with the selected intestinal gene markers (zo1: tight zonula occludens-1; zo2: tight zonula occludens-2; occludin; cla11: claudin-11; pcna: proliferating cell nuclear antigen; odc: ornithine decarboxylase; akp: alkaline phosphatase). Pearson’s correlation with the false discovery rate (FDR) of the relative abundance of gut microbiota and the selected intestinal gene markers (*, p < 0.05; **, p < 0.01).