The intestinal microbiota is considered to be a dynamic organ that plays an important role in maintaining host health, which includes Firmicutes, Bacteroidetes, Actinobacteria, Fusobacteria, and so on (Cheng et al., 2020; Wu et al., 2022). The microbiota can regulate the proliferation and differentiation of intestinal epithelial cells (IECs) and be conducive to intestinal absorption of digestible nutrients (Lin et al., 2021; Chen et al., 2021a). Moreover, intestinal flora can promote the secretion of SIgA, a very important immunoglobulin in intestinal mucosal immunity, to prevent bacterial adhesion and invasion and to maintain the integrity of the intestinal mucosal layer (Bain and Cerovic, 2020). However, studies have indicated that the disturbance of intestinal microbiota may participate in the process of disease development, such as diabetes mellitus (DM), obesity, inflammatory bowel disease (IBD), cardiovascular disease (CVD), tumor, and mental diseases (Dong et al., 2019; Villeger et al., 2019; Alvarez-Vieites et al., 2020; Suslov et al., 2021). Therefore, finding effective natural bioactive ingredients to keep the balance of intestinal microbiota is of utmost interest.

The edible basidiomycete Scorias spongiosa, which belongs to the genus Scorias Fr., (1825), was discovered by He in 2011 and is considered as a new record species after a pure culture experiment and internal transcribed spacer (ITS) sequence analysis (Zhong et al., 2020). Scorias spongiosa polysaccharides (SSPs), a chemical bioactive compound, were secreted through various stimulating agents, such as surfactants and organic solvents (Wu et al., 2018). Due to the large multitude of pharmacological activities of polysaccharides, studies have revealed that polysaccharides from natural plants have multiple effects including antioxidation, anti-inflammation, antitumor, bacteriostatic, and immune regulation (Mei et al., 2020; Wang and Liu, 2020; Ye et al., 2021; Chen et al., 2021b). However, the effect of the SSPs in alleviating gut dysbiosis has not been explored. Especially, How SSPs alter and reshape the gut microbiota remain unknown.

In the present study, we concentrated on the anti-oxidative and anti-inflammatory effects of SSPs in mice and evaluated the intestinal microbiota by 16S rDNA.

Edible fungi, which belong to the phylum fungi, can form large fleshy (or colloidal) fruiting bodies or sclerotia tissues and can be used for food or medicine (Guo et al., 2021). Polysaccharides extracted and purified from the fruiting body or mycelium have multiple physiological functions. It is reported that premna microphylla turcz leaves polysaccharides (pPMTLs) showed high anti-inflammation activity via various pathways including antimicrobial peptides (AMPs) expression pathway, immunodeficiency (IMD) pathway, target of rapamycin (TOR) pathway and intestinal autophagy pathway (Song et al., 2021). Moreover, Morchella importuna polysaccharides (MIPs) attenuate CCl₄-induced hepatic inflammatory injury via decreasing pro-inflammatory cytokine production through inhibiting the TLR4/NF-κB signaling pathway (Wen et al., 2019; Xu et al., 2021a). However, the anti-inflammatory activity of the newly found SSPs has not been evaluated. In the present study, the SSPs administration increased the anti-inflammatory cytokines content (IL-10). Contrary to the anti-inflammatory cytokines, IL-1β, IL-6, and TNF-α, as pro-inflammatory cytokines which have been reported in the intestinal inflammation occurrence (Singh et al., 2020; Kim et al., 2021), were dose-dependently decreased by SSPs administration. The results suggested that the anti-inflammation activity of SSPs was relevant to keeping the balance of pro- and anti-inflammatory cytokines.

MDA, as an indirect indicator of the degree of tissue peroxidation, can promote the infiltration of inflammatory cells and even promote the expression of myeloperoxidase (MPO), while SOD, as an antioxidant enzyme, has the opposite effect (Tsikas, 2017; Rosa et al., 2021). GSH-Px is an important enzyme that catalyzes the decomposition of hydrogen peroxide and can specifically catalyze the reduction reaction of GSH to hydrogen peroxide, which plays an important role in protecting cells and tissues from oxidative stress injury (Pu et al., 2022). In our study, the results showed that SSPs administration significantly downregulated the content of MDA and upregulated the content of GSH-Px and T-AOC. To elucidate the molecular mechanisms by which SSPs promoted the anti-oxidative capacity, we investigated the Keap1-Nrf2-ARE signaling pathway-related protein expression.

Oxidative stress refers to that when the body is stimulated, the content of reactive oxygen species (ROS) or reactive nitrogen species (RNS) free radicals exceeds the range that can be cleared by itself, resulting in the imbalance of redox balance and tissue damage, and eventually lead to a series of diseases. In response to oxidative stress, body-self-expression produces a series of endogenous antioxidant factors, including antioxidant molecules and detoxifying enzymes. Among them, the Keap1-Nrf2-ARE signaling pathway plays a crucial role in mediating endogenous antioxidant factors. The results of western blotting indicated that the SSPs administration enhanced the protein level of p-Nrf2, Keap1, and HO-1, implying that SSPs possess a strong anti-oxidant capacity via regulating the antioxidant factor production through activating the Keap1-Nrf2-ARE signaling pathway.

The human gastrointestinal (GI) tract is a huge and complex micro-ecosystem, hosting trillions of microorganisms including but not limited to bacteria, fungi, and viruses (Watanabe et al., 2021). The interactions and homeostasis among gut microorganisms, nutrient metabolism and epithelium of the GI tract are critical to host health (Motta et al., 2021). Disrupting the composition of GI microbiota may result in the development and progression of diseases. Numerous studies have demonstrated that the dysbiosis of gut bacteria may interrupt intestinal and systemic immune homeostasis, leading to the development of various kinds of diseases (Baumler and Sperandio, 2016; Sittipo et al., 2018; Chakaroun et al., 2020). As food-derived nutrients could directly interact with gut microbiota and alter the composition, diversity and function of gut bacteria, we found that SSPs-administered mice exhibit more diversity of evenness and richness than those in control mice, as they have higher Chao1 and observed_otu indices. Furthermore, the results of intestinal microbiota composition demonstrated that Firmicutes and Bacteroidota which is dominated in the gut microbiota were altered by SSPs administration. These species matter as they play a role in the body’s energy-balance mechanism as they affect energy transformation, nutrient absorption, and glucose metabolism. The Firmicutes/Bacteroidetes ratio is raised in the groups treated with SSPs. These results suggested that SSPs may regulate intestinal diversity and composition to benefit gut health.

Taken together, our study showed that SSPs are instrumental in intestinal health by enhancing the anti-inflammation and anti-oxidative capacity. Furthermore, the diversity and composition of intestinal microbiota were enriched by SSPs administration. Our findings provided a deep understanding of the benefit of polysaccharides from edible fungi as bioactive materials to intestinal health.

The datasets presented in this study can be found in online repositories. The names of the repository/repositories and accession number(s) can be found at: NCBI BioProject—PRJNA808190.

The animal study was reviewed and approved by the Animal Care and Use Committee of the Sichuan Provincial People’s Hospital (Chengdu, China).

YX, WP, and YW conceived and designed the experiments. ZZ, HF, JT, and YX conducted the experiments. YX and YW wrote the paper. YX, YC, and JZ analyzed the data. All authors contributed to the article and approved the submitted version.

This work was financially supported by the China Agriculture Research System of MOF and MARA (CARS-20).

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.