Fermentation of Pleurotus ostreatus and Ganoderma lucidum mushrooms and their extracts by the gut microbiota of healthy and osteopenic women: potential prebiotic effect and impact of mushroom fermentation products on human osteoblasts.

Evangelia N Kerezoudi,Alexandra Panagiotou,Georgios Koutrotsios,Konstantinos C Mountzouris,Ifigeneia Avgousti,Georgios I Zervakis,Evdokia K Mitsou,Katerina Gioti,Roxane Tenta,Adamantini Kyriacou,Eirini Terzi

doi:10.1039/d0fo02581j

Abstract

Recent data have highlighted the role of the gut microbiota and its several metabolites in maintaining bone health. Thus, gut microbiota manipulation, e.g., by prebiotics, might offer a plausible target in the fight against bone degenerative diseases. This study aimed (a) to investigate the in vitro prebiotic potential of Ganoderma lucidum and Pleurotus ostreatus mushrooms in healthy and osteopenic women and (b) to explore the impact of mushroom fermentation products on human osteoblasts. G. lucidum LGAM 9720 and P. ostreatus IK 1123 lyophilized mushroom-powders (2% w/v) and their hot-water extracts (1% w/v) were fermented in a 24 h static batch culture model by using faecal inocula from healthy (n = 3) or osteopenic (n = 3) donors. Gut microbiota analysis (qPCR) and measurement of short chain fatty acids (SCFAs) were performed during fermentation, and 24 h-prebiotic indexes were calculated. Evaluation of the effects of fermentation products on bone metabolism parameters (OPG: osteoprotegerin; and RANKL: receptor activator of nuclear factor kappa B ligand) in osteoblast cultures was also performed. Our data suggest that the origin of the gut microbiota inoculum plays a major role in the viability of osteoblasts. The treatments using P. ostreatus mushroom-powder and G. lucidum mushroom-extract had positive effects based on gut microbiota and SCFA analyses. Both mushrooms exhibited lower RANKL levels compared to controls, whereas their extracts tended to enhance the osteoblastic activity. In conclusion, mushrooms that are rich in beta-glucans may exert beneficial in vitro effects on bone physiology by alterations in the gut microbiota and/or SCFA production.

Highlights

The human body is the natural habitat of a large number and variety of microorganisms including bacteria, eukaryotes, archaea and viruses, widely known as “gut microbiota”
We aimed to investigate the in vitro prebiotic impact of Ganoderma lucidum and Pleurotus ostreatus mushrooms and their extracts on the gut microbiota of healthy and osteopenic women
Recent data demonstrated that gut microbiota manipulation could be a promising strategy in the prevention or/and adjuvant treatment of chronic metabolic diseases, including bone metabolism disorders

Summary

Introduction

The human body is the natural habitat of a large number and variety of microorganisms including bacteria, eukaryotes, archaea and viruses, widely known as “gut microbiota”. Declining estrogen levels result in a potent stimulation of bone resorption/osteoclastogenesis combined with a lower rate of bone formation/osteoblastogenesis leading to a period of rapid bone loss.[11] There is no single cause of osteoporosis and multiple mechanisms are involved in the pathogenesis of osteopenia. Decreased bone density has been recently correlated with gut microbiota dysregulation whereas several mechanisms have been described to support a gut–bone axis.[12] Research data have highlighted the role of the gut microbiota and its several metabolites (e.g. SCFAs) in maintaining bone health and bone mass through mechanisms including immune regulation, nutrient acquisition (calcium and phosphate), effects on gut serotonin or estrogen-like molecule production and alterations in gut barrier integrity and permeability.13–15 “osteomicrobiology” combines bone physiology, gastroenterology, immunology and microbiology in order to define the connection of the gut microbiota and bone beyond facilitating the absorption of minerals that are important for bone health.[16]

Objectives

Methods

Results

Conclusion