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Volume 167, Issue 7

Editor's Choice Phase-variable bacteria simultaneously express multiple capsules Open Access

Read the story behind the paper on the Microbe Post here.

Abstract

Capsular polysaccharides (CPSs) protect bacteria from host and environmental factors. Many bacteria can express different CPSs and these CPSs are phase variable. For example, ) is a prominent member of the human gut microbiome and expresses eight different capsular polysaccharides. Bacteria, including , have been shown to change their CPSs to adapt to various niches such as immune, bacteriophage, and antibiotic perturbations. However, there are limited tools to study CPSs and fundamental questions regarding phase variance, including if gut bacteria can express more than one capsule at the same time, remain unanswered. To better understand the roles of different CPSs, we generated a CPS1-specific antibody and a flow cytometry assay to detect CPS expression in individual bacteria in the gut microbiota. Using these novel tools, we report for the first time that bacteria can simultaneously express multiple CPSs. We also observed that nutrients such as glucose and salts had no effect on CPS expression. The ability to express multiple CPSs at the same time may provide bacteria with an adaptive advantage to thrive amid changing host and environmental conditions, especially in the intestine.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): capsular polysaccharide , microbiome and phase-variable
Funding
This study was supported by the:
  • National Institute of Diabetes and Digestive and Kidney Diseases (Award F30DK114950)
    • Principle Award Recipient: SamanthaAnne Hsieh
  • National Institute of Allergy and Infectious Diseases (Award R21AI142257)
    • Principle Award Recipient: PaulM. Allen
© 2021 The Authors
  • This is an open-access article distributed under the terms of the Creative Commons Attribution NonCommercial License.
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2021-07-05
2024-04-26
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References

  1. Hsieh SA, Allen PM. Immunomodulatory roles of polysaccharide capsules in the intestine. Front Immunol 2020; 11:690 [View Article] [PubMed]
     [Google Scholar]
  2. Porter NT, Martens EC. The critical roles of polysaccharides in gut microbial ecology and physiology. Annu Rev Microbiol 2017; 71:349–369 [View Article] [PubMed]
     [Google Scholar]
  3. Carboni F, Adamo R. Structure-based glycoconjugate vaccine design: The example of Group B streptococcus type III capsular polysaccharide. Drug Discov Today Technol 2020; 35–36:23–33 [View Article] [PubMed]
     [Google Scholar]
  4. Makela PH. Capsular polysaccharide vaccines today. Infection 1984; 12:S72–7 [View Article]
     [Google Scholar]
  5. Coyne MJ, Weinacht KG, Krinos CM, Comstock LE. Mpi recombinase globally modulates the surface architecture of a human commensal bacterium. Proc Natl Acad Sci U S A 2003; 100:10446–10451 [View Article] [PubMed]
     [Google Scholar]
  6. Hickey CA, Kuhn KA, Donermeyer DL, Porter NT, Jin C et al. Colitogenic Bacteroides thetaiotaomicron antigens access host immune cells in a sulfatase-dependent manner via outer membrane vesicles. Cell Host Microbe 2015; 17:672–680 [View Article] [PubMed]
     [Google Scholar]
  7. Li J, Zhang JR. Phase Variation of Streptococcus pneumoniae . Microbiol Spectr 2019; 7: [View Article] [PubMed]
     [Google Scholar]
  8. Chatzidaki-Livanis M, Weinacht KG, Comstock LE. Trans locus inhibitors limit concomitant polysaccharide synthesis in the human gut symbiont Bacteroides fragilis . Proc Natl Acad Sci U S A 2010; 107:11976–11980 [View Article] [PubMed]
     [Google Scholar]
  9. Martens EC, Roth R, Heuser JE, Gordon JI. Coordinate regulation of glycan degradation and polysaccharide capsule biosynthesis by a prominent human gut symbiont. J Biol Chem 2009; 284:18445–18457 [View Article] [PubMed]
     [Google Scholar]
  10. Hammerschmidt S, Muller A, Sillmann H, Muhlenhoff M, Borrow R et al. Capsule phase variation in Neisseria meningitidis serogroup B by slipped-strand mispairing in the polysialyltransferase gene (siaD): correlation with bacterial invasion and the outbreak of meningococcal disease. Mol Microbiol 1996; 20:1211–1220 [View Article] [PubMed]
     [Google Scholar]
  11. Waite RD, Penfold DW, Struthers JK, Dowson CG. Spontaneous sequence duplications within capsule genes cap8E and tts control phase variation in Streptococcus pneumoniae serotypes 8 and 37. Microbiology (Reading) 2003; 149:497–504 [View Article] [PubMed]
     [Google Scholar]
  12. Chatzidaki-Livanis M, Coyne MJ, Comstock LE. A family of transcriptional antitermination factors necessary for synthesis of the capsular polysaccharides of Bacteroides fragilis . J Bacteriol 2009; 191:7288–7295 [View Article] [PubMed]
     [Google Scholar]
  13. Srivastava M, Tucker MS, Gulig PA, Wright AC. Phase variation, capsular polysaccharide, pilus and flagella contribute to uptake of vibrio vulnificus by the eastern oyster (crassostrea virginica . Environ Microbiol 2009; 11:1934–1944 [View Article] [PubMed]
     [Google Scholar]
  14. Holst Sorensen MC, van Alphen LB, Fodor C, Crowley SM, Christensen BB et al. Phase variable expression of capsular polysaccharide modifications allows Campylobacter jejuni to avoid bacteriophage infection in chickens. Front Cell Infect Microbiol 2012; 2:11
     [Google Scholar]
  15. Wright AC, Powell JL, Tanner MK, Ensor LA, Karpas AB et al. Differential expression of Vibrio vulnificus capsular polysaccharide. Infect Immun 1999; 67:2250–2257 [View Article] [PubMed]
     [Google Scholar]
  16. Wright AC, Powell JL, Kaper JB, Morris JG. Identification of a group 1-like capsular polysaccharide operon for Vibrio vulnificus . Infect Immun 2001; 69:6893–6901 [View Article] [PubMed]
     [Google Scholar]
  17. Garrison-Schilling KL, Grau BL, McCarter KS, Olivier BJ, Comeaux NE et al. Calcium promotes exopolysaccharide phase variation and biofilm formation of the resulting phase variants in the human pathogen Vibrio vulnificus . Environ Microbiol 2011; 13:643–654 [View Article] [PubMed]
     [Google Scholar]
  18. Fernebro J, Andersson I, Sublett J, Morfeldt E, Novak R et al. Capsular expression in Streptococcus pneumoniae negatively affects spontaneous and antibiotic-induced lysis and contributes to antibiotic tolerance. J Infect Dis 2004; 189:328–338 [View Article] [PubMed]
     [Google Scholar]
  19. TerAvest MA, He Z, Rosenbaum MA, Martens EC, Cotta MA et al. Regulated expression of polysaccharide utilization and capsular biosynthesis loci in biofilm and planktonic Bacteroides thetaiotaomicron during growth in chemostats. Biotechnol Bioeng 2014; 111:165–173 [View Article] [PubMed]
     [Google Scholar]
  20. Porter NT, Luis AS, Martens EC. Bacteroides thetaiotaomicron. Trends Microbiol 2018; 26:966–967 [View Article] [PubMed]
     [Google Scholar]
  21. Kang SS, Bloom SM, Norian LA, Geske MJ, Flavell RA et al. An antibiotic-responsive mouse model of fulminant ulcerative colitis. PLoS Med 2008; 5:e41 [View Article] [PubMed]
     [Google Scholar]
  22. Xu J, Bjursell MK, Himrod J, Deng S, Carmichael LK et al. A genomic view of the human-Bacteroides thetaiotaomicron symbiosis. Science 2003; 299:2074–2076 [View Article] [PubMed]
     [Google Scholar]
  23. Porter NT, Canales P, Peterson DA, Martens EC. A subset of polysaccharide capsules in the human symbiont Bacteroides thetaiotaomicron promote increased competitive fitness in the mouse gut. Cell Host Microbe 2017; 22:494–506 [View Article] [PubMed]
     [Google Scholar]
  24. Hsieh S, Porter NT, Donermeyer DL, Horvath S, Strout G et al. Polysaccharide capsules equip the human symbiont Bacteroides thetaIotaomicron to modulate immune responses to a dominant antigen in the intestine. J Immunol 2020; 204:1035–1046 [View Article] [PubMed]
     [Google Scholar]
  25. Porter NT, Hryckowian AJ, Merrill BD, Fuentes JJ, Gardner JO et al. Phase-variable capsular polysaccharides and lipoproteins modify bacteriophage susceptibility in Bacteroides thetaiotaomicron . Nat Microbiol 2020; 5:1170–1181 [View Article] [PubMed]
     [Google Scholar]
  26. Hryckowian AJ, Merrill BD, Porter NT, Van Treuren W, Nelson EJ et al. Bacteroides thetaiotaomicron-infecting bacteriophage isolates inform sequence-based host range predictions. Cell Host Microbe 2020; 28:371–379 [View Article] [PubMed]
     [Google Scholar]
  27. Peterson DA, Planer JD, Guruge JL, Xue L, Downey-Virgin W et al. Characterizing the interactions between a naturally primed immunoglobulin A and its conserved Bacteroides thetaiotaomicron species-specific epitope in gnotobiotic mice. J Biol Chem 2015; 290:12630–12649 [View Article] [PubMed]
     [Google Scholar]
  28. Kearney JF, Radbruch A, Liesegang B, Rajewsky K. A new mouse myeloma cell line that has lost immunoglobulin expression but permits the construction of antibody-secreting hybrid cell lines. J Immunol 1979; 123:1548–1550 [PubMed]
     [Google Scholar]
  29. Wegorzewska MM, Glowacki RWP, Hsieh SA, Donermeyer DL, Hickey CA et al. Diet modulates colonic T cell responses by regulating the expression of a Bacteroides thetaiotaomicron antigen. Sci Immunol 2019; 4:32
     [Google Scholar]
  30. Loschko J, Garcia K, Cooper D, Pride M, Anderson A. Flow cytometric assays to quantify Fhbp expression and detect serotype specific capsular polysaccharides on Neisseria meningitidis . Methods Mol Biol 2019; 1969:217–236 [View Article] [PubMed]
     [Google Scholar]
  31. 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; 281:36269–36279 [View Article] [PubMed]
     [Google Scholar]
  32. Raftis EJ, Salvetti E, Torriani S, Felis GE, O’Toole PW. Genomic diversity of Lactobacillus salivarius . Appl Environ Microbiol 2011; 77:954–965 [View Article] [PubMed]
     [Google Scholar]
  33. Sonnenburg ED, Sonnenburg JL, Manchester JK, Hansen EE, Chiang HC et al. 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; 103:8834–8839 [View Article] [PubMed]
     [Google Scholar]
  34. Sonnenburg JL, Xu J, Leip DD, Chen CH, Westover BP et al. Glycan foraging in vivo by an intestine-adapted bacterial symbiont. Science 2005; 307:1955–1959 [View Article] [PubMed]
     [Google Scholar]
  35. van Hijum SA, Kralj S, Ozimek LK, Dijkhuizen L, van Geel-Schutten IG. Structure-function relationships of glucansucrase and fructansucrase enzymes from lactic acid bacteria. Microbiol Mol Biol Rev 2006; 70:157–176 [View Article] [PubMed]
     [Google Scholar]
  36. Kaluskar ZM, Garrison-Schilling KL, McCarter KS, Lambert B, Simar SR et al. Manganese is an additional cation that enhances colonial phase variation of Vibrio vulnificus . Environ Microbiol Rep 2015; 7:789–794 [View Article] [PubMed]
     [Google Scholar]
  37. Coyne MJ, Reinap B, Lee MM, Comstock LE. Human symbionts use a host-like pathway for surface fucosylation. Science 2005; 307:1778–1781 [View Article] [PubMed]
     [Google Scholar]
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Phase-variable bacteria simultaneously express multiple capsules
Microbiology 167, 001066 (2021); https://doi.org/10.1099/mic.0.001066
/content/journal/micro/10.1099/mic.0.001066
/content/journal/micro/10.1099/mic.0.001066
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