An acidic polysaccharide from Patinopecten yessoensis skirt prevents obesity and improves gut microbiota and metabolism of mice induced by high-fat diet

Highlights

• An acidic polysaccharide (SPYP) was isolated from Patinopecten yessoensis skirt.

• Main chains were elucidated as → 4)β-GlcA(1 → 4)α-GlcNAc → and → 4)β-GlcA(1 → 3)β-GalNAc→.

• SPYP could prevent obesity and hyperlipidemia induced by a high-fat diet (HFD) in mice.

• SPYP could regulate gut microbiota in HFD-fed mice, especially Lachnoclostridium.

• SPYP could affect metabolite profiles and improve lipid metabolism of HFD-mice.

Abstract

The prevention of obesity is an urgent need for worldwide public health. The scallop (Patinopecten yessoensis) skirt is the by-product of adductor processing. In order to explore the value of the scallop skirt, the present study isolated an acidic polysaccharide from the skirt of P. yessoensis (SPYP) and evaluated its anti-obesity effect. SPYP was characterized as an acidic heteropolysaccharide with a molecular weight of 13.58 kDa. Through stepwise acid hydrolysis followed by HPLC-MSⁿ analysis, two core chains in SPYP was determined as heparin-like → 4)β-GlcA(1 → 4)α-GlcNAc → and chondroitin sulfate-like → 4)β-GlcA(1 → 3)β-GalNAc →. SPYP could effectively reduce body weight, decrease fat accumulation and prevent high blood lipids induced by a high-fat diet (HFD) in mice. Further 16S ribosomal ribonucleic acid (rRNA) sequencing analysis revealed that the anti-obesity effect of SPYP was notably associated with its modulation on gut microbiota. The short-chain fatty acids were also restored by SPYP supplementation compared to the HFD group. Moreover, liquid chromatography-high resolution accurate mass spectrometry (LC-HRMS) analysis demonstrated that metabolite profiles of HFD-fed mice were altered by SPYP supplementation, especially the lipid metabolism in serum and amino acid metabolism in cecal content, which may contribute to the anti-obesity effect of SPYP. The present study offers the basis for processing and application of P. yessoensis skirt.

Introduction

Patinopecten yessoensis is one of the most important economic shellfish and is widely cultured along the coasts of China, Japan, and Russia. Commercial processing of the scallop generates a large by-product of the trimmed skirt, which pollutes the environment and causes much waste of biological resources. Therefore, utilization of this waste stream is desirable, especially as it is known to contain proteins/peptides (H. T. Wu et al., 2015), lipids (Zhou et al., 2010), and polysaccharides (B. W. Zhu et al., 2009). Moreover, the P. yessoensis skirt contains carbohydrates, protein, and lipid. To increase the economic value of P. yessoensis skirt, further development of its bioactive polysaccharides is effective. In addition, the polysaccharides from P. yessoensis skirt have proven to boost the immune response in mice (Li et al., 2021).

The natural polysaccharides from aquatic animals have a variety of biological activities, like anticoagulative (Ustyuzhanina et al., 2017), anti-oxidative (Qin et al., 2018), and osteogenic bioactivities (Song, Zhang, et al., 2018). These biological activities of polysaccharides from aquatic animals are attributed to their chemical composition and structures on account of existing glycosaminoglycan (GAG) and/or GAG-like structures (L. C. Wang et al., 2019). GAGs are participated in many biological processes, such as molecular recognition, tissue construction, defense, energy storage, and self-regulation (Cui et al., 2012, Morishita et al., 1998, Pavão, 2014). Therefore, these bioactive polysaccharides from aquatic animals are considered as potential resources to develop functional ingredients or nutraceuticals (Sun et al., 2018, Zong et al., 2012).

Due to unhealthy dietary patterns and lifestyles, obesity has become a public health problem worldwide. A high-fat diet can cause excess adipogenesis by the uptake of fatty acids from the circulation by triglycerides (TG), which leads to an increase in the size of adipocytes (Klop, Elte, & Cabezas, 2013). What’s the worse obesity is usually associated with complications such as cardiovascular diseases, diabetes, dyslipidemia, certain gastrointestinal disorders, and metabolic syndrome (Cecchini et al., 2010, Lu et al., 2016, Ogden et al., 2007). Moreover, accumulating evidence has proven that gut microbiota shows important effects on obesity (Bäckhed et al., 2007, Shen et al., 2013). In particular, the scientists have found that supplementation of the gut microbiota belonging to obese mice led to obesity in lean mice (Ley et al., 2005), suggesting that the gut microbiota can significantly influence obesity. Gut microbiota homeostasis disrupted by a high-fat diet can further induce obesity in the host due to loss of beneficial organisms, excessive growth of potentially harmful bacteria, and loss of overall microbial diversity (Cuevas-Sierra et al., 2019). In addition, dietary intervention is effective in ameliorating obesity, especially natural polysaccharides, such as sulfated polysaccharides from sea cucumber (Z. Zhu et al., 2018) and polysaccharides from Ganoderma lucidum (Chang et al., 2015). It has been well documented that indigestible polysaccharides prevent diet-induced obesity through the regulation of gut microbiota and promoting the production of short-chain fatty acids (SCFAs), which exert a role in the regulation of energy balance (Angelakis et al., 2012, Trompette et al., 2014). Furthermore, the metabolic disorders induced by obesity are also restored by polysaccharides through modulating the gut microbiota community and then influence the nutrient acquisition and energy regulation (Dethlefsen et al., 2007, Ridaura et al., 2013, Wu et al., 2019). However, further studies are needed to better understand the complex interactions among polysaccharides, gut microbiota, and metabolism.

The present study investigated the anti-obesity effect of an acidic polysaccharide isolated from the skirt of P. yessoensis (SPYP). SPYP was separated by enzymatic hydrolysis and anion-exchange resin chromatography, and its structural characteristics were analyzed by a series of chemical and spectroscopic methods. Then the anti-obesity effect of SPYP was evaluated using a mice model induced by a high-fat diet (HFD). Furthermore, the regulation of SPYP on gut microbiota and their metabolites was analyzed to explore its anti-obesity mechanism.