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      Species Deletions from Microbiome Consortia Reveal Key Metabolic Interactions between Gut Microbes

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          Abstract

          Gut microbes associate, compete for, and specialize in specific metabolic tasks. These interactions are dictated by the cross-feeding of degradation or fermentation products. However, the individual contribution of microbes to the function of the gut microbiome is difficult to evaluate. It is essential to understand the complexity of microbial interactions and how the presence or absence of specific microorganisms affects the stability and functioning of the gut microbiome. The experimental approach of this study could be used for identifying keystone species, in addition to redundant functions and conditions that contribute to community stability. Redundancy is an important feature of the microbiome, and its reduction could be useful for the design of microbial consortia with desired metabolic properties enhancing the tasks of the keystone species.

          ABSTRACT

          The gut microbiome is a complex microbial community that plays a key role in human health. Diet is an important factor dictating gut microbiome composition. This is mediated by multiple microbe-microbe interactions that result in the fermentation of nondigestible carbohydrates and the production of short-chain fatty acids. Certain species play key metabolic roles in the microbiome, and their disappearance could result in dysbiosis. In this work, a synthetic consortium of 14 gut microbes was studied during the utilization of prebiotic inulin in batch bioreactors. Fermentations were repeated leaving one species out every time, in order to evaluate the impact of their elimination on the system. Substrate consumption, microbial composition, and metabolite production were determined. Single deletions never resulted in a complete loss of bacterial growth or inulin consumption, suggesting functional redundancy. Deletions of Bacteroides dorei and Lachnoclostridium clostridioforme resulted in lower biomass and higher residual inulin. The absence of B. dorei impacted the abundance of the other 10 species negatively. Lachnoclostridium symbiosum, a butyrate producer, appeared to be the most sensitive species to deletions, being stimulated by the presence of Escherichia coli, Bifidobacterium adolescentis, B. dorei, and Lactobacillus plantarum. Conversely, bioreactors without these species did not show butyrate production. L. clostridioforme was observed to be essential for propionate production, and B. dorei for lactate production. Our analysis identified specific members that were essential for the function of the consortium. In conclusion, species deletions from microbial consortia could be a useful approach to identify relevant interactions between microorganisms and defining metabolic roles in the gut microbiome.

          IMPORTANCE Gut microbes associate, compete for, and specialize in specific metabolic tasks. These interactions are dictated by the cross-feeding of degradation or fermentation products. However, the individual contribution of microbes to the function of the gut microbiome is difficult to evaluate. It is essential to understand the complexity of microbial interactions and how the presence or absence of specific microorganisms affects the stability and functioning of the gut microbiome. The experimental approach of this study could be used for identifying keystone species, in addition to redundant functions and conditions that contribute to community stability. Redundancy is an important feature of the microbiome, and its reduction could be useful for the design of microbial consortia with desired metabolic properties enhancing the tasks of the keystone species.

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          Most cited references44

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          Intestinal Short Chain Fatty Acids and their Link with Diet and Human Health

          The colon is inhabited by a dense population of microorganisms, the so-called “gut microbiota,” able to ferment carbohydrates and proteins that escape absorption in the small intestine during digestion. This microbiota produces a wide range of metabolites, including short chain fatty acids (SCFA). These compounds are absorbed in the large bowel and are defined as 1-6 carbon volatile fatty acids which can present straight or branched-chain conformation. Their production is influenced by the pattern of food intake and diet-mediated changes in the gut microbiota. SCFA have distinct physiological effects: they contribute to shaping the gut environment, influence the physiology of the colon, they can be used as energy sources by host cells and the intestinal microbiota and they also participate in different host-signaling mechanisms. We summarize the current knowledge about the production of SCFA, including bacterial cross-feedings interactions, and the biological properties of these metabolites with impact on the human health.
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            Energy contributions of volatile fatty acids from the gastrointestinal tract in various species.

            E BERGMAN (1990)
            The VFA, also known as short-chain fatty acids, are produced in the gastrointestinal tract by microbial fermentation of carbohydrates and endogenous substrates, such as mucus. This can be of great advantage to the animal, since no digestive enzymes exist for breaking down cellulose or other complex carbohydrates. The VFA are produced in the largest amounts in herbivorous animal species and especially in the forestomach of ruminants. The VFA, however, also are produced in the lower digestive tract of humans and all animal species, and intestinal fermentation resembles that occurring in the rumen. The principal VFA in either the rumen or large intestine are acetate, propionate, and butyrate and are produced in a ratio varying from approximately 75:15:10 to 40:40:20. Absorption of VFA at their site of production is rapid, and large quantities are metabolized by the ruminal or large intestinal epithelium before reaching the portal blood. Most of the butyrate is converted to ketone bodies or CO2 by the epithelial cells, and nearly all of the remainder is removed by the liver. Propionate is similarly removed by the liver but is largely converted to glucose. Although species differences exist, acetate is used principally by peripheral tissues, especially fat and muscle. Considerable energy is obtained from VFA in herbivorous species, and far more research has been conducted on ruminants than on other species. Significant VFA, however, are now known to be produced in omnivorous species, such as pigs and humans. Current estimates are that VFA contribute approximately 70% to the caloric requirements of ruminants, such as sheep and cattle, approximately 10% for humans, and approximately 20-30% for several other omnivorous or herbivorous animals. The amount of fiber in the diet undoubtedly affects the amount of VFA produced, and thus the contribution of VFA to the energy needs of the body could become considerably greater as the dietary fiber increases. Pigs and some species of monkey most closely resemble humans, and current research should be directed toward examining the fermentation processes and VFA metabolism in those species. In addition to the energetic or nutritional contributions of VFA to the body, the VFA may indirectly influence cholesterol synthesis and even help regulate insulin or glucagon secretion. In addition, VFA production and absorption have a very significant effect on epithelial cell growth, blood flow, and the normal secretory and absorptive functions of the large intestine, cecum, and rumen. The absorption of VFA and sodium, for example, seem to be interdependent, and release of bicarbonate usually occurs during VFA absorption.(ABSTRACT TRUNCATED AT 400 WORDS)
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              Influence of diet on the gut microbiome and implications for human health

              Recent studies have suggested that the intestinal microbiome plays an important role in modulating risk of several chronic diseases, including inflammatory bowel disease, obesity, type 2 diabetes, cardiovascular disease, and cancer. At the same time, it is now understood that diet plays a significant role in shaping the microbiome, with experiments showing that dietary alterations can induce large, temporary microbial shifts within 24 h. Given this association, there may be significant therapeutic utility in altering microbial composition through diet. This review systematically evaluates current data regarding the effects of several common dietary components on intestinal microbiota. We show that consumption of particular types of food produces predictable shifts in existing host bacterial genera. Furthermore, the identity of these bacteria affects host immune and metabolic parameters, with broad implications for human health. Familiarity with these associations will be of tremendous use to the practitioner as well as the patient.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                mSystems
                mSystems
                msys
                msys
                mSystems
                mSystems
                American Society for Microbiology (1752 N St., N.W., Washington, DC )
                2379-5077
                16 July 2019
                Jul-Aug 2019
                : 4
                : 4
                : e00185-19
                Affiliations
                [a ]Department of Chemical and Bioprocess Engineering, School of Engineering, Pontificia Universidad Catolica de Chile, Santiago, Chile
                Duke University School of Medicine
                Author notes
                Address correspondence to Daniel Garrido, dgarridoc@ 123456ing.puc.cl .

                Citation Gutiérrez N, Garrido D. 2019. Species deletions from microbiome consortia reveal key metabolic interactions between gut microbes. mSystems 4:e00185-19. https://doi.org/10.1128/mSystems.00185-19.

                Author information
                https://orcid.org/0000-0002-4982-134X
                Article
                mSystems00185-19
                10.1128/mSystems.00185-19
                6635622
                31311843
                4ac7ef51-709f-40e6-98b4-545d71fe9c3b
                Copyright © 2019 Gutiérrez and Garrido.

                This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license.

                History
                : 12 March 2019
                : 26 June 2019
                Page count
                Figures: 9, Tables: 1, Equations: 0, References: 74, Pages: 16, Words: 8937
                Funding
                Funded by: MINEDUC | CONICYT | Fondo de Fomento al Desarrollo Científico y Tecnológico (FONDEF), https://doi.org/10.13039/501100008736;
                Award ID: ID16i10045
                Award Recipient : Award Recipient :
                Categories
                Research Article
                Novel Systems Biology Techniques
                Custom metadata
                July/August 2019

                bioreactor,keystone species,microbiome,butyrate,metabolic interaction

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