Gut Microbiota of Individuals Could Be Balanced by a 14-Day Supplementation With Laminaria japonica and Differed in Metabolizing Alginate and Galactofucan

Alginates are abundant marine anionic polysaccharides consumed by humans. Thus, over the years some understanding has emerged about alginate utilization by human gut microbiota (HGM). However, insights have been obtained only recently at the molecular level with regard to structure and function of alginate degrading and metabolizing enzymes from HGM. Still, numerous studies report on effects of alginates on bacterial communities from digestive tracts of various, predominantly marine organisms feeding on alginate and some of the involved alginate lyases have been characterized. Other studies describe the beneficial impact on gut microbiota elicited by alginates in animal models, for example, high-fat-diet-fed mice addressing obesity or as feed supplements for livestock. Alginates are depolymerized by a β-elimination reaction catalyzed by polysaccharide lyases (PLs) referred to as alginate lyases (ALs). The ALs are found in 15 of the 42 PL families categorized in the CAZy database. While genome mining has led to prediction of ALs encoded by bacteria of the HGM; currently, only four enzymes from this niche have been characterized biochemically and two crystal structures are reported. Alginates are composed of mannuronate (M) and guluronate (G) residues organized in M-, G-, and MG-blocks, which calls for ALs of complementary specificity to effectively depolymerize alginate to alginate oligosaccharides (AOSs) and monosaccharides. Typically, ALs of different PL families are encoded by genes arranged in clusters denoted as polysaccharide utilization loci. Currently, biochemical and structural analyses of marine bacterial ALs contribute to depicting the mode of action of predicted enzymes from bacteria of the HGM.

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Gut bacterial alginate degrading enzymes

Madsen

Tandrup

Wilkens

et al. 2023

Essays in Biochemistry

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Potential use of seaweed polysaccharides as prebiotics for management of metabolic syndrome: a review

Wang

Zhang

Chang

et al. 2023

Critical Reviews in Food Science and Nutrition

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Metagenomic insights into the dynamic degradation of brown algal polysaccharides by kelp-associated microbiota

Zhang,

Zhao

et al. 2024

Appl Environ Microbiol

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Marine bacteria play important roles in the degradation and cycling of algal polysaccharides. However, the dynamics of epiphytic bacterial communities and their roles in algal polysaccharide degradation during kelp decay are still unclear. Here, we performed metagenomic analyses to investigate the identities and predicted metabolic abilities of epiphytic bacterial communities during the early and late decay stages of the kelp Saccharina japonica . During kelp decay, the dominant epiphytic bacterial communities shifted from Gammaproteobacteria to Verrucomicrobia and Bacteroidetes. In the early decay stage of S. japonica , epiphytic bacteria primarily targeted kelp-derived labile alginate for degradation, among which the gammaproteobacterial Vibrionaceae (particularly Vibrio ) and Psychromonadaceae (particularly Psychromonas ), abundant in alginate lyases belonging to the polysaccharide lyase (PL) families PL6, PL7, and PL17, were key alginate degraders. More complex fucoidan was preferred to be degraded in the late decay stage of S. japonica by epiphytic bacteria, predominantly from Verrucomicrobia (particularly Lentimonas ), Pirellulaceae of Planctomycetes (particularly Rhodopirellula ), Pontiellaceae of Kiritimatiellota, and Flavobacteriaceae of Bacteroidetes, which depended on using glycoside hydrolases (GHs) from the GH29, GH95, and GH141 families and sulfatases from the S1_15, S1_16, S1_17, and S1_25 families to depolymerize fucoidan. The pathways for algal polysaccharide degradation in dominant epiphytic bacterial groups were reconstructed based on analyses of metagenome-assembled genomes. This study sheds light on the roles of different epiphytic bacteria in the degradation of brown algal polysaccharides. IMPORTANCE Kelps are important primary producers in coastal marine ecosystems. Polysaccharides, as major components of brown algal biomass, constitute a large fraction of organic carbon in the ocean. However, knowledge of the identities and pathways of epiphytic bacteria involved in the degradation process of brown algal polysaccharides during kelp decay is still elusive. Here, based on metagenomic analyses, the succession of epiphytic bacterial communities and their metabolic potential were investigated during the early and late decay stages of Saccharina japonica . Our study revealed a transition in algal polysaccharide-degrading bacteria during kelp decay, shifting from alginate-degrading Gammaproteobacteria to fucoidan-degrading Verrucomicrobia, Planctomycetes, Kiritimatiellota, and Bacteroidetes. A model for the dynamic degradation of algal cell wall polysaccharides, a complex organic carbon, by epiphytic microbiota during kelp decay was proposed. This study deepens our understanding of the role of epiphytic bacteria in marine algal carbon cycling as well as pathogen control in algal culture.

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Gut Microbiota of Individuals Could Be Balanced by a 14-Day Supplementation With Laminaria japonica and Differed in Metabolizing Alginate and Galactofucan

Cited by 3 publications

References 50 publications

Gut bacterial alginate degrading enzymes

Gut bacterial alginate degrading enzymes

Potential use of seaweed polysaccharides as prebiotics for management of metabolic syndrome: a review

Metagenomic insights into the dynamic degradation of brown algal polysaccharides by kelp-associated microbiota

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