1,848
Views
1
CrossRef citations to date
0
Altmetric
Research Paper

Dietary sugars silence the master regulator of carbohydrate utilization in human gut Bacteroides species

ORCID Icon, ORCID Icon & ORCID Icon
Article: 2221484 | Received 22 Dec 2022, Accepted 08 May 2023, Published online: 26 Jun 2023

References

  • Matijašić M, Meštrović T, Perić M, Čipčić Paljetak H, Panek M, Vranešić Bender D, Ljubas Kelečić D, Krznarić Ž, Verbanac D. Modulating composition and metabolic activity of the gut microbiota in IBD patients. Int J Mol Sci. 2016;17(4):1–19. PubMed Central PMCID: PMC4849034. doi:10.3390/ijms17040578.
  • Frank DN, St. Amand AL, Feldman RA, Boedeker EC, Harpaz N, Pace NR. Molecular-phylogenetic characterization of microbial community imbalances in human inflammatory bowel diseases. Proc Natl Acad Sci U S A. 2007;104(34):13780–13785. PubMed Central PMCID: PMC1959459. doi:10.1073/pnas.0706625104.
  • Ott SJ, Musfeldt M, Wenderoth DF, Hampe J, Brant O, Fölsch UR, Timmis KN, Schreiber S. Reduction in diversity of the colonic mucosa associated bacterial microflora in patients with active inflammatory bowel disease. Gut. 2004;53(5):685–693. PubMed Central PMCID: PMC1774050. doi:10.1136/gut.2003.025403.
  • Kowalska-Duplaga K, Gosiewski T, Kapusta P, Sroka-Oleksiak A, Wędrychowicz A, Pieczarkowski S, Ludwig-Słomczyńska AH, Wołkow PP, Fyderek K. Differences in the intestinal microbiome of healthy children and patients with newly diagnosed Crohn’s disease. Sci Rep. 2019;9(1):1–11. PubMed Central PMCID: PMC6906406. doi:10.1038/s41598-019-55290-9.
  • Liu W, Zhang R, Shu R, Yu J, Li H, Long H, Jin S, Li S, Hu Q, Yao F, et al. Study of the relationship between microbiome and colorectal cancer susceptibility using 16SrRNA sequencing. Hindawi Biomed Res Int. 2020;2020:1–17. PubMed Central PMCID: PMC7011317. doi:10.1155/2020/7828392.
  • Milani C, Ticinesi A, Gerritsen J, Nouvenne A, Lugli GA, Mancabelli L, Turroni F, Duranti S, Mangifesta M, Viappiani A, et al. Gut microbiota composition and clostridium difficile infection in hospitalized elderly individuals: a metagenomic study. Sci Rep. 2016;6(1):1–12. PubMed Central PMCID: PMC4863157. doi:10.1038/srep25945.
  • Mathew S, Smatti MK, Al Ansari K, Nasrallah GK, Al Thani AA, Yassine HM. Mixed viral-bacterial infections and their effects on gut microbiota and clinical illnesses in children. Sci Rep. 2019;9(1):1–12. PubMed Central PMCID: PMC6351549. doi:10.1038/s41598-018-37162-w.
  • Rao SSC, Rehman A, Yu S, de Andino NM. Brain fogginess, gas and bloating: a link between SIBO, probiotics and metabolic acidosis. Clin Transl Gastroenterol. 2018;9(6):1–9. PubMed Central PMCID: PMC6006167. doi:10.1038/s41424-018-0030-7.
  • Desai MS, Seekatz AM, Koropatkin NM, Kamada N, Hickey CA, Wolter M, Pudlo NA, Kitamoto S, Terrapon N, Muller A, et al. A dietary fiber-deprived gut microbiota degrades the colonic mucus barrier and enhances pathogen susceptibility. Cell. 2016;167(5):1339–1353.e21. PubMed Central PMCID: PMC5131798. doi:10.1016/j.cell.2016.10.043.
  • Shahanshah Khan SW, Godfrey V, Abdul Wadud Khan M, Ramachandran RA, Cantarel BL, Behrendt C, Peng L, Hooper LV, Zaki H, Zaki H. Dietary simple sugars alter microbial ecology in the gut and promote colitis in mice. Sci Transl Med. 2020;12(567). doi: 10.1126/scitranslmed.aay6218.
  • David LA, Maurice CF, Carmody RN, Gootenberg DB, Button JE, Wolfe BE, Ling AV, Devlin AS, Varma Y, Fischbach MA, et al. Diet rapidly and reproducibly alters the human gut microbiome. Nature. 2014 Jan 23;505(7484):559–563. PubMed Central PMCID: PMC3957428. doi:10.1038/nature12820.
  • Wu M, McNulty NP, Rodionov DA, Khoroshkin MS, Griffin NW, Cheng J, Latreille P, Kerstetter RA, Terrapon N, Henrissat B, et al. Genetic determinants of in vivo fitness and diet responsiveness in multiple human gut Bacteroides. Science. 2015;350(6256). PubMed Central PMCID: PMC4608238. doi:10.1126/science.aac5992.
  • Shepherd ES, DeLoache WC, Pruss KM, Whitaker WR, Sonnenburg JL. An exclusive metabolic niche enables strain engraftment in the gut microbiota. Nature. 2018 May;557(7705):434–438. PubMed Central PMCID: PMC6126907. doi:10.1038/s41586-018-0092-4.
  • Pudlo NAU, Karthik C, Ryan P, Ali A, Todd J, Roberto T, Nicolas H, Bernard P, Daniel Z, Cherie S, et al. Phenotypic and genomic diversification in complex carbohydrate-degrading human gut bacteria. mSystems. 2022;7(1). PubMed Central PMCID: PMC8845570. doi:10.1128/msystems.00947-21.
  • Bjursell MK, Martens EC, Gordon JI. Functional genomic and metabolic studies of the adaptations of a prominent adult human gut symbiont, Bacteroides thetaiotaomicron, to the suckling period. J Biol Chem. 2006;281(47):36269–36279. doi:10.1074/jbc.M606509200.
  • Martens EC, Chiang HC, Gordon JI. Mucosal glycan foraging enhances fitness and transmission of a saccharolytic human gut bacterial symbiont. Cell Host & Microbe. 2008 Nov 13;4(5):447–457. PubMed Central PMCID: PMC2605320. doi:10.1016/j.chom.2008.09.007.
  • Sonnenburg ED, Zheng H, Joglekar P, Higginbottom SK, Firbank SJ, Bolam DN, Sonnenburg JL. Specificity of polysaccharide use in intestinal bacteroides species determines diet-induced microbiota alterations. Cell. 2010;141(7):1241–1252. PubMed Central PMCID: PMC2900928. doi:10.1016/j.cell.2010.05.005.
  • Zmora N, Suez J, Elinav E. You are what you eat: diet, health and the gut microbiota. Nat Rev Gastroenterol Hepatol. 2019 Jan;16(1):35–56. doi:10.1038/s41575-018-0061-2.
  • Townsend GE, Han W, Schwalm ND, Raghavan V, Barry NA, Goodman AL, Groisman EA. Dietary sugar silences a colonization factor in a mammalian gut symbiont. Proc Natl Acad Sci USA. 2018;116(1):233–238. PubMed Central PMCID: PMC6320540. doi:10.1073/pnas.1813780115.
  • Wegorzewska MM, Glowacki RWP, Hsieh SA, Donermeyer DL, Hickey CA, Horvath SC, Martens EC, Stappenbeck TS, Allen PM. Diet modulates colonic T cell responses by regulating the expression of a Bacteroides thetaiotaomicron antigen. Sci Immunol. 2019;4(32):1–13. PubMed Central PMCID: PMC6550999. doi:10.1126/sciimmunol.aau9079.
  • Sonnenburg ED, Sonnenburg JL, Manchester JK, Hansen EE, Chiang HC, Gordon JI. A hybrid two-component system protein of a prominent human gut symbiont couples glycan sensing in vivo to carbohydrate metabolism. Proc Natl Acad Sci U S A. 2006;103(23):8834–8839. PubMed Central PMCID: PMC1472243. doi:10.1073/pnas.0603249103.
  • Townsend GE, Raghavan V, Zwir I, Groisman EA. Intramolecular arrangement of sensor and regulator overcomes relaxed specificity in hybrid two-component systems. Proc Natl Acad Sci U S A. 2013;110(2):E161–E169. PubMed Central PMCID: PMC3545799. doi:10.1073/pnas.1212102110.
  • Cordain LE, Boyd S, Sebastian A, Mann N, Lindeberg S, Watkins BA, O’Keefe JH, Brand-Miller J. Origins and evolution of the western diet: health implications for the 21st century [Commentary]. Am J Clin Nutr. 2005 Feb 1; 81(2):341–354. doi:10.1093/ajcn.81.2.341.
  • Fajstova A, Galanova N, Coufal S, Malkova J, Kostovcik M, Cermakova M, Pelantova H, Kuzma M, Sediva B, Hudcovic T, et al. Diet rich in simple sugars promotes pro-inflammatory response via gut microbiota alteration and TLR4 signaling. Cells. 2020 Dec 16;9(12):2701. PubMed Central PMCID: PMC7766268. doi:10.3390/cells9122701.
  • Kawano Y, Edwards M, Huang Y, Bilate AM, Araujo LP, Tanoue T, Atarashi K, Ladinsky MS, Reiner SL, Wang HH, et al. Microbiota imbalance induced by dietary sugar disrupts immune-mediated protection from metabolic syndrome. Cell. 2022 Sep 15;185(19):3501–3519 e20. PubMed Central PMCID: PMC9556172. doi:10.1016/j.cell.2022.08.005.
  • Schwalm ND, Townsend GE, Groisman EA, Comstock LE, Shuman HA. Multiple signals govern utilization of a polysaccharide in the gut bacterium Bacteroides thetaiotaomicron. mBio. 2016;7(5):1–9. PubMed Central PMCID: PMC5061871. doi:10.1128/mbio.01342-16.
  • Townsend GE, Han W, Schwalm ND, Hong X, Bencivenga-Barry NA, Goodman AL, Groisman EA. A master regulator of bacteroides thetaiotaomicron gut colonization controls carbohydrate utilization and an alternative protein synthesis factor. mBio. 2020;11(1):1–14. PubMed Central PMCID: PMC6989115. doi:10.1128/mBio.03221-19.
  • Schwalm ND, Townsend GE, Groisman EA. Prioritization of polysaccharide utilization and control of regulator activation in Bacteroides thetaiotaomicron. Mol Microbiol. 2017;104(1):32–45. doi:10.1111/mmi.13609.
  • Glowacki RWP, Pudlo NA, Tuncil Y, Luis AS, Sajjakulnukit P, Terekhov AI, Lyssiotis CA, Hamaker BR, Martens EC. A ribose-scavenging system confers colonization fitness on the human gut symbiont bacteroides thetaiotaomicron in a diet-specific manner. Cell Host & Microbe. 2020;27(1):79–92.e9. PubMed Central PMCID: PMC7031954. doi:10.1016/j.chom.2019.11.009.
  • Martens EC, Lowe EC, Chiang H, Pudlo NA, Wu M, McNulty NP, Abbott DW, Henrissat B, Gilbert HJ, Bolam DN, et al. Recognition and degradation of plant cell wall polysaccharides by two human gut symbionts. PLoS Biol. 2011;9(12):e1001221. PubMed Central PMCID: PMC3243724. doi:10.1371/journal.pbio.1001221.
  • Lowe EC, Basle A, Czjzek M, Firbank SJ, Bolam DN. A scissor blade-like closing mechanism implicated in transmembrane signaling in a Bacteroides hybrid two-component system. Proc Natl Acad Sci U S A. 2012 May 8;109(19):7298–7303. PubMed Central PMCID: PMC3358863. doi:10.1073/pnas.1200479109.
  • Ryan D, Jenniches L, Reichardt S, Barquist L, Westermann AJ. A high-resolution transcriptome map identifies small RNA regulation of metabolism in the gut microbe Bacteroides thetaiotaomicron. Nat Commun. 2020;11(1). PubMed Central PMCID: PMC7366714. doi:10.1038/s41467-020-17348-5.
  • Cao Y, Förstner KU, Vogel J, Smith CJ. Cis-encoded small RNAs, a conserved mechanism for repression of polysaccharide utilization in Bacteroides. J Bacteriol. 2016;198(18):2410–2418. PubMed Central PMCID: PMC4999932. doi:10.1128/JB.00381-16.
  • Ryan D, Bornet E, Prezza G, Alampalli SV, de Carvalho TF, Felchle H, Ebbecke T, Hayward R, Deutschbauer AM, Barquist L, Westermann AJ. An integrated transcriptomics-functional genomics approach reveals a small RNA that modulates Bacteroides thetaiotaomicron sensitivity to tetracyclines. bioRxiv. 2023 Feb 16. PubMed Central PMCID: PMC9949090. doi:10.1101/2023.02.16.528795.
  • Adams AND, Azam MS, Costliow ZA, Ma X, Degnan PH, Vanderpool CK. A novel family of RNA-Binding proteins regulate polysaccharide metabolism in Bacteroides thetaiotaomicron. J Bacteriol. 2021 Oct 12;203(21):e0021721. PubMed Central PMCID: PMC8508124. doi:10.1128/JB.00217-21.
  • Krypotou E, Townsend GE, Gao X, Tachiyama S, Liu J, Pokorzynski ND, Goodman AL, Groisman EA. Bacteria require phase separation for fitness in the mammalian gut. Science. 2023 Mar 17;379(6637):1149–1156. PubMed Central PMCID: PMC10148683. doi:10.1126/science.abn7229.
  • Krinos CMC, Michael J, Weinacht K, Tzianabos G, Arthur O, Kasper DL, Comstock LE. Extensive surface diversity of a commensal microorganism by multiple DNA inversions. Nature. 2001;414(6863):555–558. doi:10.1038/35107092.
  • Cerdeńo-Tãrraga AM, Patrick S, Crossman LC, Blakely G, Abratt V, Lennard N, Poxton I, Duerden B, Harris B, Quail MA, et al. Extensive DNA inversions in the B. fragilis genome control variable gene expression. Science. 2005 Mar 4;307(5714):1463–1465. PubMed PMID: 15746427. doi:10.1126/science.1107008.
  • Cho KH, Cho D, Wang GR, Salyers AA. New regulatory gene that contributes to control of Bacteroides thetaiotaomicron starch utilization genes. J Bacteriol. 2001 Dec;183(24):7198–7205. PubMed Central PMCID: PMC95569. doi:10.1128/JB.183.24.7198-7205.2001.
  • Han W, Peng BZ, Wang C, Townsend GE, Barry NA, Peske F, Goodman AL, Liu J, Rodnina MV, Groisman EA. Gut colonization by Bacteroides requires translation by an EF-G paralog lacking GTPase activity. EMBO J. 2022 Dec 6:e112372. PubMed Central PMCID: PMC9841332. doi:10.15252/embj.2022112372.
  • Ravcheev DA, Godzik A, Osterman AL, Rodionov DA. Polysaccharides utilization in human gut bacterium Bacteroides thetaiotaomicron: comparative genomics reconstruction of metabolic and regulatory networks. Bmc Genom. 2013;14(1):1–17. PubMed Central PMCID: PMC3878776. doi:10.1186/1471-2164-14-873.
  • Modesto JL, Pearce VH, Townsend GE. 2nd Harnessing gut microbes for glycan detection and quantification. Nat Commun. 2023 Jan 17;14(1):275. PubMed Central PMCID: PMC9845299. doi:10.1038/s41467-022-35626-2.
  • Terrapon N, Lombard V, Drula E, Lapébie P, Al-Masaudi S, Gilbert HJ, Henrissat B. PULDB: the expanded database of polysaccharide utilization loci. Nucleic Acids Res. 2018 Jan 4;46(D1):D677–D683. PubMed Central PMCID: PMC5753385. doi:10.1093/nar/gkx1022.
  • Busby SE, Richard H. Transcription activation by catabolite activator protein (CAP). J Mol Biol. 1999;293(2):199–213. doi:10.1006/jmbi.1999.3161.
  • Iyer R, Baliga NS, Camilli A. Catabolite control protein a (CcpA) contributes to virulence and regulation of sugar metabolism in streptococcus pneumoniae. J Bacteriol. 2005 Dec;187(24):8340–8349. PubMed Central PMCID: PMC1317011. doi:10.1128/JB.187.24.8340-8349.2005.
  • Deutscher J, Francke C, Postma PW. How phosphotransferase system-related protein phosphorylation regulates carbohydrate metabolism in bacteria. Microbiol Mol Biol Rev. 2006 Dec;70(4):939–1031. PubMed Central PMCID: PMC1698508. doi:10.1128/MMBR.00024-06.
  • Siegel LS, Hylemon PB, Phibbs PV. Cyclic adenosine 3‘,5’-monophosphate levels and activities of adenylate cyclase and cyclic adenosine 3‘,5’-monophosphate phosphodiesterase in pseudomonas and Bacteroides. J Bacteriol. 1977;129(1):87–96. PubMed Central PMCID: PMC234899. doi:10.1128/jb.129.1.87-96.1977.
  • Han S, Van Treuren W, Fischer CR, Merrill BD, DeFelice BC, Sanchez JM, Higginbottom SK, Guthrie L, Fall LA, Dodd D, et al. A metabolomics pipeline for the mechanistic interrogation of the gut microbiome. Nature. 2021 Jul;595(7867):415–420. PubMed Central PMCID: PMC8939302. doi:10.1038/s41586-021-03707-9.
  • Liu H, Shiver AL, Price MN, Carlson HK, Trotter VV, Chen Y, Escalante V, Ray J, Hern KE, Petzold CJ. et al. Functional genetics of human gut commensal Bacteroides thetaiotaomicron reveals metabolic requirements for growth across environments. Cell Rep. 2021 Mar 2;34(9):108789. PubMed Central PMCID: PMC8121099. doi:10.1016/j.celrep.2021.108789.
  • Goodman AL, McNulty NP, Zhao Y, Leip D, Mitra RD, Lozupone CA, Knight R, Gordon JI. Identifying genetic determinants needed to establish a human gut symbiont in its habitat. Cell Host & Microbe. 2009 Sep 17;6(3):279–289. PubMed Central PMCID: PMC2895552. doi:10.1016/j.chom.2009.08.003.
  • Liou CS, Sirk SJ, Diaz CAC, Klein AP, Fischer CR, Higginbottom SK, Erez A, Donia MS, Sonnenburg JL, Sattely ES, et al. A metabolic pathway for activation of dietary glucosinolates by a human gut symbiont. Cell. 2020 Feb 20;180(4):717–728.e19. PubMed Central PMCID: PMC7515767. doi:10.1016/j.cell.2020.01.023.
  • Wexler AG, Goodman AL. An insider’s perspective: Bacteroides as a window into the microbiome. Nat Microbiol. 2017;2(April):1–11. PubMed Central PMCID: PMC5679392. doi:10.1038/nmicrobiol.2017.26.
  • Crouch LI, Liberato MV, Urbanowicz PA, Baslé A, Lamb CA, Stewart CJ, Cooke K, Doona M, Needham S, Brady RR. et al. Prominent members of the human gut microbiota express endo-acting O-glycanases to initiate mucin breakdown. Nat Commun. 2020 Aug 11;11(1):4017. PubMed Central PMCID: PMC7419316. doi:10.1038/s41467-020-17847-5.
  • Raghavan V, Lowe EC, Townsend GE, Bolam DN, Groisman EA. Tuning transcription of nutrient utilization genes to catabolic rate promotes growth in a gut bacterium. Mol Microbiol. 2014 Sep;93(5):1010–1025. doi:10.1111/mmi.12714.
  • Pudlo NA, Urs K, Kumar SS, German JB, Mills DA, Martens EC. Symbiotic human gut bacteria with variable metabolic priorities for host mucosal glycans. mBio. 2015;6(6):e01282–15. PubMed Central PMCID: PMC4659458. doi:10.1128/mBio.01282-15.
  • Degnan PH, Barry NA, Mok KC, Taga M, Goodman A. Human gut microbes use multiple transporters to distinguish vitamin B12 analogs and compete in the gut. Cell Host & Microbe. 2014 Jan 15;15(1):47–57. PubMed Central PMCID: PMC3923405. doi:10.1016/j.chom.2013.12.007.
  • Costliow ZA, Degnan PH, Vanderpool CK. Thiamine pyrophosphate riboswitches in Bacteroides species regulate reanscription or translation of tiamine transport and biosynthesis genes. bio Rxiv. 2019. doi:10.1101/867226.
  • Costliow ZA, Degnan PH. Thiamine acquisition strategies impact metabolism and competition in the gut microbe Bacteroides thetaiotaomicron. mSystems. 2017;2(5). PubMed Central PMCID: PMC5613172. doi:10.1128/msystems.00116-17.
  • King AM, Vanderpool CK, PH D, Ellermeier CD. sRNA target prediction organizing tool (SPOT) integrates computational and experimental data to facilitate functional characterization of bacterial small RNAs. mSphere. 2019 Jan 30;4(1). PubMed Central PMCID: PMC6354806. doi:10.1128/mSphere.00561-18.
  • Donaldson GP, Chou WC, Manson AL, Rogov P, Abeel T, Bochicchio J, Ciulla D, Melnikov A, Ernst PB, Chu H, et al. Spatially distinct physiology of Bacteroides fragilis within the proximal colon of gnotobiotic mice. Nat Microbiol. 2020;5(5):746–756. PubMed Central PMCID: PMC7426998. doi:10.1038/s41564-020-0683-3.
  • Comstock LE, Silhavy TJ. Small RNAs repress expression of polysaccharide utilization loci of gut Bacteroides species. J Bacteriol. 2016;198(18):2396–2398. PubMed Central PMCID: PMC4999925. doi:10.1128/jb.00514-16.
  • McCown PJ, Corbino KA, Stav S, Sherlock ME, Breaker RR. Riboswitch diversity and distribution. RNA. 2017 Jul;23(7):995–1011. PubMed Central PMCID: PMC5473149. doi:10.1261/rna.061234.117.
  • Bencivenga-Barry NA, Lim B, Herrera CM, Trent MS, Goodman AL. Genetic manipulation of wild human gut bacteroides. J Bacteriol. 2020;202(3). PubMed Central PMCID: PMC6964735. doi:10.1128/JB.00544-19.
  • García-Bayona L, Comstock LE, Lemon KP. Streamlined genetic manipulation of diverse bacteroides and parabacteroides isolates from the human gut microbiota. mBio. 2019;10(4). PubMed Central PMCID: PMC6692515. doi:10.1128/mBio.01762-19.
  • Koropatkin NM, Martens EC, Gordon JI, Smith TJ. Starch catabolism by a prominent human gut symbiont is directed by the recognition of amylose helices. Structure. 2008 Jul;16(7):1105–1115. PubMed Central PMCID: PMC2563962. doi:10.1016/j.str.2008.03.017.
  • Perez JC, Shin D, Zwir I, Latifi T, Hadley TJ, Groisman EA. Evolution of a bacterial regulon controlling virulence and Mg(2+) homeostasis. PLoS Genet. 2009 Mar;5(3):e1000428. PubMed Central PMCID: PMC2650801. doi:10.1371/journal.pgen.1000428.
  • Mann M, Wright PR, Backofen R. IntaRNA 2.0: enhanced and customizable prediction of RNA-RNA interactions. Nucleic Acids Res. 2017 Jul 3;45(W1):W435–W439. PubMed Central PMCID: PMC5570192. doi:10.1093/nar/gkx279.