Elsevier

Food Bioscience

Volume 50, Part B, December 2022, 102116
Food Bioscience

Effects of exopolysaccharides from Antrodia cinnamomea on inflammation and intestinal microbiota disturbance induced by antibiotics in mice

https://doi.org/10.1016/j.fbio.2022.102116Get rights and content

Abstract

Antrodia cinnamomea is an important edible and medicinal mushroom, and it exhibits multiple biological activities, such as hepatoprotection, antitumor, antivirus, and immunoregulation. Polysaccharides are the main products of A. cinnamomea in submerged fermentation. In this work, exopolysaccharides from A. cinnamomea (AEPS) were extracted and purified by alcohol precipitation and Sevag method. Composition analysis revealed that AEPS were primarily composed of three distinct polysaccharides with mean molecular weights of 1,013, 233, and 28,743 kDa, accounting for 78%, 18%, and 4% of AEPS, respectively. The AEPS have β-type glycosidic bonds and relatively strong resistance to digestion. In vivo experiments showed that the intragastric administration of AEPS in mice with medium dose (0.25 g/kg body weight of mice) has the following effects: remarkably alleviate lincomycin hydrochloride (LIH)-induced injuries to immune organs; enhance the relative abundance of beneficial microorganisms such as Lactobacillus, Roseburia, Ligilactobacillus, and Lachnospiraceae_NK4A136_group in the intestinal tract; greatly reduce the levels of inflammatory cytokines IL-6 and TNF-α in serum and the relative abundances of harmful microbes such as Enterococcus and Shigella; regulate the balance of the gut microflora; and relieve LIH-induced symptoms such as diarrhea, inflammation, and weight loss. These findings might represent a new alternative to develop novel multifunctional carbohydrate prebiotics.

Introduction

The intestinal system is a microbial ecosystem containing many microbes that contribute to the development and function of the mucosal immune system (Ouwehand et al., 2002). Gut microbes are closely related to alimentation and body immunity (Zhao et al., 2022), and they can directly affect the state and function of intestinal mucosa, thereby influencing the functions of other organs and the health of the organism. Thus, regulating the gut microbial composition and maintaining the balance of gut microbiota are some of the effective ways to maintain a healthy status. Antibiotics are commonly used to treat diseases, but their long-term use easily disrupts the integrity of the useful gut microbiota (Blaser, 2011) and increases the abundance of drug-fast harmful microbes, that lead to a dramatic increase in the risk of antibiotic-associated diarrhea and other chronic diseases (Gao et al., 2017; Pelaseyed & Hansson, 2020). Even the short-term use of antibiotics may cause the presence of drug-resistant bacteria in the human gut system for years (Jakobsson et al., 2010). Therefore, regulating and maintaining the homeostasis of microbiota disturbed by antibiotics are vital for human health.

Prebiotics can modulate antibiotic-induced gut microbiota disturbance (Ladirat et al., 2014). Beta-glucan in fungi is a potential high-quality prebiotic (Aida et al., 2009). Polysaccharides in fungi can regulate gut microbiota and play a prebiotic role by selectively stimulating the growth of one or more microbes in the intestinal tract, thereby promoting the health of the host (Kothari et al., 2018). Antrodia cinnamomea (syn. Antrodia camphorata) is emerging edible and medicinal fungi, and it belongs to Antrodia, Polyporales, and Basidiomycota (Chen et al., 2022). Over 200 kinds of chemical compounds are extracted from the fruiting bodies or mycelia of A. cinnamomea (Kuang et al., 2021), including triterpene, polysaccharide, and maleic acid, succinic acid, and ubiquinone derivatives. These substances exhibit various bioactivities, such as anti-inflammatory (Yang, Wang, et al., 2022), antitumor (Huang et al., 2022), antidiabetic (Kuang et al., 2022), hepatoprotective (Xu et al., 2022), and immunoregulatory (Liao et al., 2022).

A. cinnamomea exopolysaccharides (AEPS) are the main product of A. cinnamomea in submerged fermentation. Current reports on AEPS focus on boosting its yield (Lee et al., 2022) or exploring its bioactivities (Yang, Han, et al., 2022). However, few studies focus on its regulatory effect on the gut microbiota. In the present work, the regulatory effect of AEPS on the gut microbiota and treatment of antibiotic-induced symptoms (diarrhea, inflammation, and weight loss) in mice were primarily investigated to provide a new perspective and a theoretical basis for developing new multifunctional prebiotics.

Section snippets

Strains and animal

A. cinnamomea strain (ATCC 200183) was purchased from American Type Culture Collection (USA). All ICR mice (6 weeks old, 20 ± 2 g, male) were provided by the Comparative Medical Center of Yangzhou University (Yangzhou University, Yangzhou, Jiangsu, China). All animal procedures were in accordance with the guidelines issued by the Ethics Committee of Laboratory Animals, Yangzhou University (SYXK2016-0019).

Extraction and purification of AEPS

The AEPS was extracted and purified according to the method reported by Li et al. (2015).

Composition of AEPS

As shown in Table 1, the content of neutral polysaccharides and protein in AEPS was 88.74% ± 0.53% and 1.21% ± 0.14%, indicating that the purity of AEPS was high enough for in vivo experiments (Bie et al., 2021). In addition, AEPS primarily contains five monosaccharides: glucose (84.73%), galactose (7.84%), mannose (5.27%), galacturonic acid (0.76%), and glucuronic acid (1.4%).

Composition and in vitro resistance digestion of AEPS

The high-performance gel filtration chromatography showed that AEPS primarily consists of three kinds of

Conclusions

AEPS primarily consists of three kinds of polysaccharides, whose molecular weights were 1,013, 233, and 28,743 kDa. It belongs to β-type glucoside, and it has a strong resistance to digestion. In vivo experiment showed that AEPS can alleviate LIH-induced adverse symptoms, such as diarrhea, inflammation, weight loss, and injuries to immune organs in mice. The medium dose (0.25 g/kg bw) gavage of AEPS could regulate the composition and balance of the gut microflora in mice by increasing the

Author statement

Funding acquisition, Huaxiang Li and Yilin Ren; Investigation and Data curation, Chunlei Lu; Methodology and Writing—original draft, Huaxiang Li; Software and visualization, Yilin Ren; Conceptualization and writing—review and editing, Byong H. Lee; supervision and project administration, Zhenquan Yang; Validation, Dan Ji; Resources, Shengqi Rao. All authors have read and agreed to the published version of the manuscript.

Declaration of competing interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Acknowledgement

This work was financially supported by the National Natural Science Foundation of China (Grant numbers: 32001661 and 32101964), and the Natural Science Foundation of Jiangsu Province, China (Grant number: BK20190890).

References (47)

  • Y. Yang et al.

    A homogeneous polysaccharide from Lycium barbarum: Structural characterizations, anti-obesity effects and impacts on gut microbiota

    International Journal of Biological Macromolecules

    (2021)
  • S. Zong et al.

    Chemical compositions, anti-oxidant and anti-inflammatory potential of ethanol extract from Zhuke-Hulu tea

    Food Bioscience

    (2021)
  • J.S. Ayres et al.

    Lethal inflammasome activation by a multidrug-resistant pathobiont upon antibiotic disruption of the microbiota

    Nature Medicine

    (2012)
  • J.R. Bedarf et al.

    Functional implications of microbial and viral gut metagenome changes in early-stage L-DOPA-naïve Parkinson's disease patients

    Genome Medicine

    (2017)
  • N.N. Bie et al.

    Regulatory effect of non-starch polysaccharides from purple sweet potato on intestinal microbiota of mice with antibiotic-associated diarrhea

    Food & Function

    (2021)
  • M. Blaser

    Stop the killing of beneficial bacteria

    Nature

    (2011)
  • P.D. Cani et al.

    Next-generation beneficial microbes: The case of Akkermansia muciniphila

    Frontiers in Microbiology

    (2017)
  • C.L. Chen et al.

    Sexual crossing, chromosome-level genome sequences, and comparative genomic analyses for the medicinal mushroom Taiwanofungus camphoratus (Syn. Antrodia Cinnamomea, Antrodia Camphorata)

    Microbiology Spectrum

    (2022)
  • M.S. Desai et al.

    A dietary fiber-deprived gut microbiota degrades the colonic mucus barrier and enhances pathogen susceptibility

    Cell

    (2016)
  • N. Dey et al.

    Association of gut microbiota with post-operative clinical course in Crohn's disease

    BMC Gastroenterology

    (2013)
  • M.S. Dong et al.

    Determination of the extraction, physicochemical characterization, and digestibility of sulfated polysaccharides in seaweed — Porphyra haitanensis

    Marine Drugs

    (2020)
  • B.P. Ganesh et al.

    Commensal Akkermansia muciniphila exacerbates gut inflammation in Salmonella Typhimurium-infected gnotobiotic mice

    PLoS One

    (2013)
  • P.F. Gao et al.

    Feed-additive probiotics accelerate yet antibiotics delay intestinal microbiota maturation in broiler chicken

    Microbiome

    (2017)
  • Cited by (5)

    View full text