cis-encoded small RNAs, a conserved mechanism for repression of polysaccharide utilization in Bacteroides

Journal of Bacteriology

Volumn 198, Issue 18, 2016, Pages 2410-2418

  Cao, Yanlu ^a,c   Förstner, Konrad U ^b   Vogel, Jörg ^b   Jeffrey Smith, C ^a  

^a EAST CAROLINA UNIVERSITY   (United States)

^b UNIVERSITY OF WÜRZBURG   (Germany)

^c DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENTARY RNA; GLYCAN; POLYSACCHARIDE; RNA; SMALL RNA; TRANSCRIPTOME; UNCLASSIFIED DRUG; BACTERIAL RNA; SIGMA FACTOR; SMALL INTERFERING RNA;

ARTICLE; BACTEROIDES FRAGILIS; CATABOLITE REPRESSION; CONTROLLED STUDY; GENE CLUSTER; GENE EXPRESSION; GENETIC CONSERVATION; GENETIC REGULATION; INTESTINE FLORA; NONHUMAN; POLYSACCHARIDE UTILIZATION LOCUS; PRIORITY JOURNAL; RNA SEQUENCE; RNA TRANSCRIPTION; BACTEROIDES; DOWN REGULATION; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PHYSIOLOGY; RNA INTERFERENCE;

BACTEROIDES; DOWN-REGULATION; GENE EXPRESSION REGULATION, BACTERIAL; POLYSACCHARIDES; RNA INTERFERENCE; RNA, BACTERIAL; RNA, SMALL INTERFERING; SIGMA FACTOR;

EID: 84984908623     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.00381-16     Document Type: Article

References (44)

1. McNeil NI. 1984. The contribution of the large intestine to energy supplies in man. Am J Clin Nutr 39:338-342.
2. Nobel YR, Cox LM, Kirigin FF, Bokulich NA, Yamanishi S, Teitler I, Chung J, Sohn J, Barber CM, Goldfarb DS, Raju K, Abubucker S, Zhou Y, Ruiz VE, Li H, Mitreva M, Alekseyenko AV, Weinstock GM, Sodergren E, Blaser MJ. 2015. Metabolic and metagenomic outcomes from early-life pulsed antibiotic treatment. Nat Commun 6:7486. http://dx.doi.org/10.1038/ncomms8486.
3. Round JL, Mazmanian SK. 2009. The gut microbiota shapes intestinal immune responses during health and disease. Nat Rev Immunol 9:313-323. http://dx.doi.org/10.1038/nri2515.
4. Sommer F, Backhed F. 2013. The gut microbiota-masters of host development and physiology. Nat Rev Microbiol 11:227-238. http://dx.doi.org/10.1038/nrmicro2974.
5. Tremaroli V, Backhed F. 2012. Functional interactions between the gut microbiota and host metabolism. Nature 489:242-249. http://dx.doi.org/10.1038/nature11552.
6. Brook I. 1988. Recovery of anaerobic bacteria from clinical specimens in 12 years at two military hospitals. J Clin Microbiol 26:1181-1188.
7. Eckburg PB, Bik EM, Bernstein CN, Purdom E, Dethlefsen L, Sargent M, Gill SR, Nelson KE, Relman DA. 2005. Diversity of the human intestinal microbial flora. Science 308:1635-1638. http://dx.doi.org/10.1126/science.1110591.
8. Faith JJ, Guruge JL, Charbonneau M, Subramanian S, Seedorf H, Goodman AL, Clemente JC, Knight R, Heath AC, Leibel RL, Rosenbaum M, Gordon JI. 2013. The long-term stability of the human gut microbiota. Science 341:1237439. http://dx.doi.org/10.1126/science .1237439.
9. Lassmann B, Gustafson DR, Wood CM, Rosenblatt JE. 2007. Reemergence of anaerobic bacteremia. Clin Infect Dis 44:895-900. http://dx.doi.org/10.1086/512197.
10. Vena A, Munoz P, Alcala L, Fernandez-Cruz A, Sanchez C, Valerio M, Bouza E. 2015. Are incidence and epidemiology of anaerobic bacteremia really changing? Eur J Clin Microbiol Infect Dis 34:1621-1629. http://dx.doi.org/10.1007/s10096-015-2397-7.
11. Cao Y, Rocha ER, Smith CJ. 2014. Efficient utilization of complex Nlinked glycans is a selective advantage for Bacteroides fragilis in extraintestinal infections. Proc Natl Acad Sci U S A 111:12901-12906. http://dx.doi.org/10.1073/pnas.1407344111.
12. Krinos CM, Coyne MJ, Weinacht KG, Tzianabos AO, Kasper DL, Comstock LE. 2001. Extensive surface diversity of a commensal microorganism by multiple DNA inversions. Nature 414:555-558. http://dx.doi.org/10.1038/35107092.
13. Polk BF, Kasper DL. 1977. Bacteroides fragilis subspecies in clinical isolates. Ann Intern Med 86:569-571. http://dx.doi.org/10.7326/0003-4819-86-5-569.
14. 2: the role of OxyR and its effect on survival and virulence. Mol Microbiol 67:129-142.
15. Koropatkin NM, Cameron EA, Martens EC. 2012. How glycan metabolism shapes the human gut microbiota. Nat Rev Microbiol 10:323-335.
16. Martens EC, Chiang HC, Gordon JI. 2008. Mucosal glycan foraging enhances fitness and transmission of a saccharolytic human gut bacterial symbiont. Cell Host Microbe 4:447-457. http://dx.doi.org/10.1016/j .chom.2008.09.007.
17. Sonnenburg ED, Zheng H, Joglekar P, Higginbottom SK, Firbank SJ, Bolam DN, Sonnenburg JL. 2010. Specificity of polysaccharide use in intestinal Bacteroides species determines diet-induced microbiota alterations. Cell 141:1241-1252. http://dx.doi.org/10.1016/j.cell.2010.05.005.
18. Xu J, Bjursell MK, Himrod J, Deng S, Carmichael LK, Chiang HC, Hooper LV, Gordon JI. 2003. A genomic view of the human-Bacteroides thetaiotaomicron symbiosis. Science 299:2074-2076. http://dx.doi.org/10.1126/science.1080029.
19. Tancula E, Feldhaus MJ, Bedzyk LA, Salyers AA. 1992. Location and characterization of genes involved in binding of starch to the surface of Bacteroides thetaiotaomicron. J Bacteriol 174:5609-5616.
20. Martens EC, Koropatkin NM, Smith TJ, Gordon JI. 2009. Complex glycan catabolism by the human gut microbiota: the Bacteroidetes Suslike paradigm. J Biol Chem 284:24673-24677. http://dx.doi.org/10.1074/jbc.R109.022848.
21. Rogers TE, Pudlo NA, Koropatkin NM, Bell JS, Moya Balasch M, Jasker K, Martens EC. 2013. Dynamic responses of Bacteroides thetaiotaomicron during growth on glycan mixtures. Mol Microbiol 88:876-890. http://dx.doi.org/10.1111/mmi.12228.
22. Pudlo NA, Urs K, Kumar SS, German JB, Mills DA, Martens EC. 2015. Symbiotic human gut bacteria with variable metabolic priorities for host mucosal glycans. mBio 6(6):e01282-15. http://dx.doi.org/10.1128/mBio .01282-15.
23. Lynch JB, Sonnenburg JL. 2012. Prioritization of a plant polysaccharide over a mucus carbohydrate is enforced by a Bacteroides hybrid twocomponent system. Mol Microbiol 85:478-491. http://dx.doi.org/10.1111/j.1365-2958.2012.08123.x.
24. Baughn AD, Malamy MH. 2002. A mitochondrial-like aconitase in the bacterium Bacteroides fragilis: implications for the evolution of the mitochondrial Krebs cycle. Proc Natl Acad Sci U S A 99:4662-4667. http://dx.doi.org/10.1073/pnas.052710199.
25. Smith CJ, Rogers MB, McKee ML. 1992. Heterologous gene expression in Bacteroides fragilis. Plasmid 27:141-154. http://dx.doi.org/10.1016/0147-619X(92)90014-2.
26. Privitera G, Dublanchet A, Sebald M. 1979. Transfer of multiple antibiotic resistance between subspecies of Bacteroides fragilis. J Infect Dis 139:97-101. http://dx.doi.org/10.1093/infdis/139.1.97.
27. Rocha ER, Smith CJ. 1997. Regulation of Bacteroides fragilis katB mRNA by oxidative stress and carbon limitation. J Bacteriol 179:7033-7039.
28. Varel VH, Bryant MP. 1974. Nutritional features of Bacteroides fragilis sp. fragilis. Appl Microbiol 28:251-257.
29. Sharma CM, Hoffmann S, Darfeuille F, Reignier J, Findeiss S, Sittka A, Chabas S, Reiche K, Hackermuller J, Reinhardt R, Stadler PF, Vogel J. 2010. The primary transcriptome of the major human pathogen Helicobacter pylori. Nature 464:250-255. http://dx.doi.org/10.1038/nature08756.
30. Sharma CM, Vogel J. 2014. Differential RNA-seq: the approach behind and the biological insight gained. Curr Opin Microbiol 19:97-105. http://dx.doi.org/10.1016/j.mib.2014.06.010.
31. Förstner KU, Vogel J, Sharma CM. 2014. READemption-a tool for the computational analysis of deep-sequencing-based transcriptome data. Bioinformatics 30:3421-3423. http://dx.doi.org/10.1093/bioinformatics/btu533.
32. Hoffmann S, Otto C, Kurtz S, Sharma CM, Khaitovich P, Vogel J, Stadler PF, Hackermuller J. 2009. Fast mapping of short sequences with mismatches, insertions and deletions using index structures. PLoS Comput Biol 5:e1000502. http://dx.doi.org/10.1371/journal.pcbi.1000502.
33. Nicol JW, Helt GA, Blanchard SG, Jr, Raja A, Loraine AE. 2009. The Integrated Genome Browser: free software for distribution and exploration of genome-scale datasets. Bioinformatics 25:2730-2731. http://dx.doi.org/10.1093/bioinformatics/btp472.
34. Caswell CC, Gaines JM, Ciborowski P, Smith D, Borchers CH, Roux CM, Sayood K, Dunman PM, Roop RM, II. 2012. Identification of two small regulatory RNAs linked to virulence in Brucella abortus 2308. Mol Microbiol 85:345-360. http://dx.doi.org/10.1111/j.1365-2958.2012.08117.x.
35. Bayley DP, Rocha ER, Smith CJ. 2000. Analysis of cepA and other Bacteroides fragilis genes reveals a unique promoter structure. FEMS Microbiol Lett 193:149-154. http://dx.doi.org/10.1111/j.1574-6968.2000.tb09417.x.
36. Chen S, Bagdasarian M, Kaufman MG, Bates AK, Walker ED. 2007. Mutational analysis of the ompA promoter from Flavobacterium johnsoniae. J Bacteriol 189:5108-5118. http://dx.doi.org/10.1128/JB.00401-07.
37. Brantl S. 2007. Regulatory mechanisms employed by cis-encoded antisense RNAs. Curr Opin Microbiol 10:102-109. http://dx.doi.org/10.1016/j.mib.2007.03.012.
38. Georg J, Hess WR. 2011. cis-Antisense RNA, another level of gene regulation in bacteria. Microbiol Mol Biol Rev 75:286-300. http://dx.doi.org/10.1128/MMBR.00032-10.
39. Kelley LA, Mezulis S, Yates CM, Wass MN, Sternberg MJ. 2015. The Phyre2 web portal for protein modeling, prediction and analysis. Nat Protoc 10:845-858. http://dx.doi.org/10.1038/nprot.2015.053.
40. Mitchell A, Chang HY, Daugherty L, Fraser M, Hunter S, Lopez R, McAnulla C, McMenamin C, Nuka G, Pesseat S, Sangrador-Vegas A, Scheremetjew M, Rato C, Yong SY, Bateman A, Punta M, Attwood TK, Sigrist CJ, Redaschi N, Rivoire C, Xenarios I, Kahn D, Guyot D, Bork P, Letunic I, Gough J, Oates M, Haft D, Huang H, Natale DA, Wu CH, Orengo C, Sillitoe I, Mi H, Thomas PD, Finn RD. 2015. The InterPro protein families database: the classification resource after 15 years. Nucleic Acids Res 43:D213-D221. http://dx.doi.org/10.1093/nar/gku1243.
41. Martens EC, Roth R, Heuser JE, Gordon JI. 2009. Coordinate regulation of glycan degradation and polysaccharide capsule biosynthesis by a prominent human gut symbiont. J Biol Chem 284:18445-18457. http://dx.doi.org/10.1074/jbc.M109.008094.
42. Wegmann U, Horn N, Carding SR. 2013. Defining the bacteroides ribosomal binding site. Appl Environ Microbiol 79:1980-1989. http://dx.doi.org/10.1128/AEM.03086-12.
43. Lee SM, Donaldson GP, Mikulski Z, Boyajian S, Ley K, Mazmanian SK. 2013. Bacterial colonization factors control specificity and stability of the gut microbiota. Nature 501:426-429. http://dx.doi.org/10.1038/nature12447.
44. Salyers AA, West SE, Vercellotti JR, Wilkins TD. 1977. Fermentation of mucins and plant polysaccharides by anaerobic bacteria from the human colon. Appl Environ Microbiol 34:529-533.