Microbiota-accessible carbohydrates

Microbiota-accessible carbohydrates (MACs) are carbohydrates that are resistant to digestion by a host's metabolism, and are made available for gut microbes, as prebiotics, to ferment or metabolize into beneficial compounds, such as short chain fatty acids.[1] The term, ‘‘microbiota-accessible carbohydrate’’ contributes to a conceptual framework for investigating and discussing the amount of metabolic activity that a specific food or carbohydrate can contribute to a host's microbiota.[1]

MACs may come from plants, fungi, animal tissues, or food-borne microbes, and must be metabolized by the microbiome.[1] A significant quantity of the cellulose humans consume is not metabolized by gut microbes and therefore cannot be considered a MAC.[2] The amount of dietary MACs found within a food source will differ for each individual, since which carbohydrates are metabolized depends upon the composition of each person's microbiota. For example, many Japanese individuals possess the genes for the consumption of the algal polysaccharide porphyran in their microbiomes, which are rarely found in North American and European individuals.[3][4] For individuals who harbor such a porphyran-degrading strain, porphyran would be a MAC. However, porphyran would not be a MAC for those without a microbiota adaptation to seaweed. In similar fashion, germ-free mice without a microbiota might consume a diet with large quantities of potential MACs, but none of the carbohydrates would be considered MACs, since they would escape the digestive tract without being metabolized by microbes.[1]

Lack of dietary MACs results in a microbiota reliant upon endogenous host-derived MACs, such as mucin glycans.[5] Different host genotypes can influence the identity of MACs available to the microbiota in multiple ways. For example, a host's genes may affect the level of mucus structures, such as the absence of alpha-1-2 fucose residues in the mucus of nonsecretor individuals who lack alpha-1-2- fucosyltransferase activity in the intestine.[6] Similarly, a host may have genes that can determine the efficiency of digestion and absorption of carbohydrates in the small intestine. For example, lactose is accessible to the microbiota in people who are lactose intolerant, and should therefore be considered a MAC for those individuals. For nursing infants, dietary MACs that are naturally found in breast milk are known as human milk oligosaccharides (HMOs).[7][8][9] For formula-fed infants, dietary MACs, such as galacto-oligosaccharides, are artificially added to formula.[10] Therefore, the research, discussion and quantification of MACs and their impact on a host's microbiota may be critical to determining their impact on human health.[1]

Gut microbiota diversity

Diets in developed countries have lost microbiota-accessible carbohydrates which is the cause of a substantial depletion of gut microbiota taxa. This loss of microbiota diversity is likely involved in the increasing propensity for a broad range of inflammatory diseases, such as allergic disease, asthma, inflammatory bowel disease (IBD), obesity, and associated noncommunicable diseases (NCDs). Rural human communities from South America and Africa have a low prevalence of NCDs and this fact has been related with a higher gut microbiota diversity.[11] Some of these lost taxa belong to the families of Bacteroidales (Bacteroides fragilis, B. ovatus, B. uniformis, B. distasonis, Parabacteroides gordonii), Clostridiales (Ruminococcus gnavus, Blautia producta, Faecalibacterium prausnitzii) and Verrucomicrobiales (Akkermansia muciniphila). Introduction of dietary MACs in the diet is insufficient to regain the lost taxa, to restore the gut microbiota to its original state requires the administration of missing taxa, which can be achieved either by administering probiotics (food) or live biotherapeutics (drugs), in combination with dietary MAC consumption. Enriching the food supply with dietary fiber might have an essential role in preventing loss of certain beneficial bacterial species.[12]

References

  1. 1 2 3 4 5 Sonnenburg, Erica D.; Sonnenburg, Justin L. (2014). "Starving our Microbial Self: The Deleterious Consequences of a Diet Deficient in Microbiota-Accessible Carbohydrates". Cell Metabolism. 20 (5): 779–786. doi:10.1016/j.cmet.2014.07.003. ISSN 1550-4131. PMC 4896489. PMID 25156449.
  2. ↑ Chassard, Christophe; Delmas, Eve; Robert, Céline; Bernalier-Donadille, Annick (2010). "The cellulose-degrading microbial community of the human gut varies according to the presence or absence of methanogens". FEMS Microbiology Ecology. 74 (1): 205–213. doi:10.1111/j.1574-6941.2010.00941.x. ISSN 0168-6496. PMID 20662929.
  3. ↑ Hehemann, Jan-Hendrik; Correc, Gaëlle; Barbeyron, Tristan; Helbert, William; Czjzek, Mirjam; Michel, Gurvan (2010). "Transfer of carbohydrate-active enzymes from marine bacteria to Japanese gut microbiota". Nature. 464 (7290): 908–912. Bibcode:2010Natur.464..908H. doi:10.1038/nature08937. ISSN 0028-0836. PMID 20376150. S2CID 2820027.
  4. ↑ Hehemann, J.-H.; Kelly, A. G.; Pudlo, N. A.; Martens, E. C.; Boraston, A. B. (2012). "Bacteria of the human gut microbiome catabolize red seaweed glycans with carbohydrate-active enzyme updates from extrinsic microbes". Proceedings of the National Academy of Sciences. 109 (48): 19786–19791. Bibcode:2012PNAS..10919786H. doi:10.1073/pnas.1211002109. ISSN 0027-8424. PMC 3511707. PMID 23150581.
  5. ↑ Sonnenburg, J. L. (2005). "Glycan Foraging in Vivo by an Intestine-Adapted Bacterial Symbiont". Science. 307 (5717): 1955–1959. Bibcode:2005Sci...307.1955S. doi:10.1126/science.1109051. ISSN 0036-8075. PMID 15790854. S2CID 13588903.
  6. ↑ Kashyap, P. C.; Marcobal, A.; Ursell, L. K.; Smits, S. A.; Sonnenburg, E. D.; Costello, E. K.; Higginbottom, S. K.; Domino, S. E.; Holmes, S. P.; Relman, D. A.; Knight, R.; Gordon, J. I.; Sonnenburg, J. L. (2013). "Genetically dictated change in host mucus carbohydrate landscape exerts a diet-dependent effect on the gut microbiota". Proceedings of the National Academy of Sciences. 110 (42): 17059–17064. Bibcode:2013PNAS..11017059K. doi:10.1073/pnas.1306070110. ISSN 0027-8424. PMC 3800993. PMID 24062455.
  7. ↑ Bode, L. (2012). "Human milk oligosaccharides: Every baby needs a sugar mama". Glycobiology. 22 (9): 1147–1162. doi:10.1093/glycob/cws074. ISSN 0959-6658. PMC 3406618. PMID 22513036.
  8. ↑ Marcobal, Angela; Barboza, Mariana; Sonnenburg, Erica D.; Pudlo, Nicholas; Martens, Eric C.; Desai, Prerak; Lebrilla, Carlito B.; Weimer, Bart C.; Mills, David A.; German, J. Bruce; Sonnenburg, Justin L. (2011). "Bacteroides in the Infant Gut Consume Milk Oligosaccharides via Mucus-Utilization Pathways". Cell Host & Microbe. 10 (5): 507–514. doi:10.1016/j.chom.2011.10.007. ISSN 1931-3128. PMC 3227561. PMID 22036470.
  9. ↑ Marcobal, A; Kashyap, P C; Nelson, T A; Aronov, P A; Donia, M S; Spormann, A; Fischbach, M A; Sonnenburg, J L (2013). "A metabolomic view of how the human gut microbiota impacts the host metabolome using humanized and gnotobiotic mice". The ISME Journal. 7 (10): 1933–1943. doi:10.1038/ismej.2013.89. ISSN 1751-7362. PMC 3965317. PMID 23739052.
  10. ↑ Alliet, Philippe; Scholtens, Petra; Raes, Marc; Hensen, Karen; Jongen, Hanne; Rummens, Jean-Luc; Boehm, Guenther; Vandenplas, Yvan (2007). "Effect of prebiotic galacto-oligosaccharide, long-chain fructo-oligosaccharide infant formula on serum cholesterol and triacylglycerol levels". Nutrition. 23 (10): 719–723. doi:10.1016/j.nut.2007.06.011. ISSN 0899-9007. PMID 17664059.
  11. ↑ "Conserving and restoring the human gut microbiome by increasing consumption of dietary fibre - Gut Microbiota for Health". 9 May 2016. Retrieved 16 June 2016.
  12. ↑ Sonnenburg, Erica D.; Smits, Samuel A.; Tikhonov, Mikhail; Higginbottom, Steven K.; Wingreen, Ned S.; Sonnenburg, Justin L. (14 January 2016). "Diet-induced extinctions in the gut microbiota compound over generations". Nature. 529 (7585): 212–215. Bibcode:2016Natur.529..212S. doi:10.1038/nature16504. PMC 4850918. PMID 26762459.
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