Dietary macroalgae enhances amino acid metabolism via intestinal Shewanella in grass carp (Ctenopharyngodon idella)

Abstract

The gut microbiome plays pivotal roles in the host’s metabolic response to dietary interventions. Dietary macroalgae supplementation represents a promising strategy for enhancing animal growth and health via microbiome modulation. However, the underlying mechanism of how macroalgae supplementation regulates microbiome-host interactions in aquatic species remains unclear. This study investigated the effects of three dietary macroalgae—Sargassum hemiphyllum (S), Asparagopsis taxiformis (A), and Gracilaria lemaneiformis (G)—each supplemented at 5% in feed, on the gut microbiome and metabolism of grass carp (Ctenopharyngodon idella), using integrated approaches of 16S rRNA sequencing, metagenomics, and metabolomics. While all three macroalgae influenced host growth, supplementation of S provided the most comprehensive benefits, with significant enhancement of body weight and hepatic superoxide dismutase activity. Integrated multi-omics analysis revealed that dietary macroalgae supplementation increased the relative abundance of the key gut bacterial genus Shewanella, with the most notable effect observed in the supplementation of S. Subsequent analysis of a metagenome-assembled genome (MAG) of Shewanella (MAG C3_bin52) demonstrated its considerable potential for amino acid biosynthesis and metabolism. This genomic potential was further supported by metabolomic profiling, which indicated significant upregulation of amino acid-related metabolites, particularly in the supplementation S. Pathway analysis confirmed enrichment in processes associated with protein digestion and absorption, amino acid biosynthesis, and related metabolic pathways. These findings highlight the modulation of a macroalgae-microbiome-metabolite axis in grass carp, primarily mediated by the enrichment of Shewanella in gut ecosystem for enhancing host amino acid metabolism. This study advances understanding of dietary modulation of the gut microbiome and provides insights for the sustainable development of aquaculture.

Keywords

Amino acid metabolism / Grass carp (Ctenopharyngodon idella) / Gut microbiome / Macroalgae / Shewanella

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Funding

Zhuhai Industry-University-Research Cooperation Project(2320004002504)

Southern Marine Science and Engineering Guangdong Laboratory (Zhuhai)(SML2021SP203)

RIGHTS & PERMISSIONS

The Author(s)