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The Influence of Probiotics on the Firmicutes/Bacteroidetes Ratio In microorganisms Review The Influence of Probiotics on the Firmicutes/Bacteroidetes Ratio in the Treatment of Obesity and Inflammatory Bowel disease Spase Stojanov 1,2, Aleš Berlec 1,2 and Borut Štrukelj 1,2,* 1 Faculty of Pharmacy, University of Ljubljana, SI-1000 Ljubljana, Slovenia; [email protected] (S.S.); [email protected] (A.B.) 2 Department of Biotechnology, Jožef Stefan Institute, SI-1000 Ljubljana, Slovenia * Correspondence: borut.strukelj@ffa.uni-lj.si Received: 16 September 2020; Accepted: 31 October 2020; Published: 1 November 2020 Abstract: The two most important bacterial phyla in the gastrointestinal tract, Firmicutes and Bacteroidetes, have gained much attention in recent years. The Firmicutes/Bacteroidetes (F/B) ratio is widely accepted to have an important influence in maintaining normal intestinal homeostasis. Increased or decreased F/B ratio is regarded as dysbiosis, whereby the former is usually observed with obesity, and the latter with inflammatory bowel disease (IBD). Probiotics as live microorganisms can confer health benefits to the host when administered in adequate amounts. There is considerable evidence of their nutritional and immunosuppressive properties including reports that elucidate the association of probiotics with the F/B ratio, obesity, and IBD. Orally administered probiotics can contribute to the restoration of dysbiotic microbiota and to the prevention of obesity or IBD. However, as the effects of different probiotics on the F/B ratio differ, selecting the appropriate species or mixture is crucial. The most commonly tested probiotics for modifying the F/B ratio and treating obesity and IBD are from the genus Lactobacillus. In this paper, we review the effects of probiotics on the F/B ratio that lead to weight loss or immunosuppression. Keywords: probiotics; Firmicutes; Bacteroidetes; dysbiosis; obesity; inflammation 1. Introduction In the human body,trillions of microorganisms live in symbiosis with the host and are mainly located in the gastrointestinal tract, skin, saliva, oral mucosa, conjunctiva, and vagina [1]. Microorganisms that inhabit the gastrointestinal tract (i.e., gut microbiota) number approximately 1 1014 [2] and play an × essential role in intestinal homeostasis, development, and protection against pathogens. Furthermore, their presence in the gut is associated with immunomodulatory and metabolic reactions [3]. Gut microbiota consists of bacteria, yeasts, and viruses. Bacteria in the gut are represented by more than 1000 species that belong to six dominant phyla: Firmicutes, Bacteroidetes, Actinobacteria, Proteobacteria, Fusobacteria, and Verrucomicrobia. Bacteria from the phyla Firmicutes and Bacteroidetes are the most common, representing 90% of the gut microbiota [4]. The gut microbiota of a healthy individual differs in different parts of the gastrointestinal tract and changes with time due to aging (including infant development) and environmental factors such as dietary habits, lifestyle, and antibiotic consumption. Large differences in microbiota composition exist among individuals, with the differences attributed to age, ethnicity, lifestyle, and diet [4,5]. Different microbiota are classified into three distinct enterotypes [6]. Such variations are considered physiological and consistent with healthy microbiota. Nevertheless, changes in microbiota composition are often related to diseases, also termed dysbioses. However, the causality between altered microbiota and various diseases is often unclear. Microorganisms 2020, 8, 1715; doi:10.3390/microorganisms8111715 www.mdpi.com/journal/microorganisms Microorganisms 2020, 8, 1715 2 of 16 Microorganisms 2020, 8, x FOR PEER REVIEW 2 of 15 To somewhat simplify the complex issue of microbiota composition, the present review only addressedTo somewhat the two majorsimplify bacterial the complex phyla inissue the of gastrointestinal microbiota composition, tract: Firmicutes the present and Bacteroidetes. review only Theaddressed ratio between the two these major two bacterial phyla (thephyla Firmicutes in the gastro/Bacteroidetesintestinal (Ftract:/B) ratio)Firmicutes has been and associated Bacteroidetes. with maintainingThe ratio between homeostasis, these two and phyla changes (the Firmicutes/Bac in this ratio canteroidetes lead to (F/B) various ratio) pathologies. has been associated For example, with increasesmaintaining in thehomeostasis, abundance and of specific changes Firmicutes in this rati oro Bacteroidetescan lead to various species pathologies. lead to obesity For and example, bowel inflammation,increases in the respectively abundance [of7, 8specific]. The phylum Firmicutes Firmicutes or Bacteroidetes includes Gram-positivespecies lead to bacteriaobesity and with bowel rigid orinflammation, semi-rigidcell respectively walls that [7,8]. are predominantlyThe phylum Firmic fromutes the includes genera BacillusGram-posit, Clostridiumive bacteria, Enterococcus with rigid, Lactobacillusor semi-rigid, andcell Ruminicoccuswalls that are[4 predominantly,9], whilst the phylum from the Bacteroidetes genera Bacillus includes, Clostridium approximately, Enterococcus 7000, diLactobacillusfferent species, and of Ruminicoccus Gram-negative [4,9], bacteria whilst that the are phylum predominantly Bacteroidetes from theincludes genera approximatelyBacteroides, Alistipes 7000, Parabacteroidesdifferent species, and ofPrevotella Gram-negative[10]. Although bacteriathere that isare much predominantly focus on the from F/B ratio, the genera one should Bacteroides bear in, mindAlistipes that, Parabacteroides this ratio can, be and aff Prevotellaected by an[10]. increase Although in other there phyla is much and focus that on dysbiotic the F/B increases ratio, one in should other phylabear in do mind not that necessarily this ratio change can be the affected F/B ratio. by an The increase most in variable other phyla phylum and was that demonstrated dysbiotic increases to be Proteobacteria,in other phyla do which not necessarily contributes change to dysbiosis the F/B [11 ]ra andtio. isThe correlated most variable with a phylum decrease was in Firmicutes demonstrated and generalto be Proteobacteria, microbial diversity which in inflammatorycontributes to bowel dysbiosis disease [11] (IBD) and [ 12is]. correlated with a decrease in FirmicutesBalancing and thegeneral intestinal microbial ecosystem diversity is anin importantinflammatory aspect bowel of maintainingdisease (IBD) normal [12]. human body function,Balancing and manythe intestinal therapeutic ecosystem strategies is an are important designed aspect to achieve of maintaining an appropriate normal F /humanB ratio. body The administrationfunction, and many of probiotics, therapeutic prebiotics, strategies synbiotics, are designed phage therapy,to achieve fecal an transplantation, appropriate F/B and ratio. bacterial The consortiumadministration transplantation of probiotics, haveprebiotics, all been synbiotics, tested as phage methods therapy, to modulate fecal transplantation, gut microbiota and [ 13bacterial]. The presentconsortium review transplantation thus also focuses have on al thel been use of tested probiotics as methods for balancing to mo thedulate F/B ratiogut microbiota and, consequentially, [13]. The treatingpresent obesityreview andthus IBD. also focuses on the use of probiotics for balancing the F/B ratio and, consequentially,Accordingto treating the WHO obesity definition, and IBD. probiotics are live microorganisms that can confer health benefitsAccording to the host to the when WHO administered definition, in probiotics adequate amounts. are live microorganisms By modifying the that microbiota, can confer probiotics health canbenefits potentially to the host treat when several administered diseases [in14 adequate] and exert amounts. anti-obesity By modifying and anti-inflammatory the microbiota, eprobioticsffects [7]. Ascan illustrated potentially in treat Figure several1, probiotics diseases contribute [14] and exert to the anti-obesity alteration and of the anti-inflammatory F /B ratio, thereby effects influencing [7]. As hostillustrated obesity in or Figure intestinal 1, probiotics inflammation. contribute The aimto the of alteration this review of wasthe F/B to elucidate ratio, thereby the eff influencingects of different host probioticobesity or species intestinal on obesityinflammation. and inflammation The aim of as this well review as their was relationship to elucidate with the the effects F/B ratio. of different probiotic species on obesity and inflammation as well as their relationship with the F/B ratio. Figure 1. ChangesChanges in the the Firmicutes/Bacteroidetes Firmicutes/Bacteroidetes (F(F/B)/B) ratio can cause obesity or inflammatory inflammatory bowel disease. Specific probiotics can restore the gut microbial balance by influencing the F/B ratio. means↑ disease. Specific probiotics can restore the gut microbial balance by influencing the F/B ratio." increase; means↓ decrease. means increase;# means decrease. 2. The Role of Gut Microbiota in Nutrition and Obesity Microorganisms 2020, 8, 1715 3 of 16 2. The Role of Gut Microbiota in Nutrition and Obesity The gut microbiota plays an essential role in food digestion due to the presence of genes, which encode digestive enzymes that are not present in human cells, but are associated with the metabolism and fermentation of several food compounds that present nutritional benefits to the host. The most abundant metabolic products of gut microbiota are short-chain fatty acids (SCFAs), mainly acetate, propionate, and
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