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Group B Streptococcus cpsE Is Required for Serotype V Capsule Production and Aids in Biofilm Formation and Ascending Infection of the Reproductive Tract during Pregnancy

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Download Hi-Res ImageDownload to MS-PowerPointCite This:ACS Infect. Dis. 2021, 7, 9, 2686-2696
    Article

    Group B Streptococcus cpsE Is Required for Serotype V Capsule Production and Aids in Biofilm Formation and Ascending Infection of the Reproductive Tract during Pregnancy
    Click to copy article linkArticle link copied!

    • Kristen Noble
      Kristen Noble
      Department of Pediatrics, Vanderbilt University School of Medicine, Nashville, Tennessee 37212, United States
      More by Kristen Noble
    • Jacky Lu
      Jacky Lu
      Department of Pathology, Microbiology and Immunology, Vanderbilt University Medical Center, Nashville, Tennessee 37212, United States
      More by Jacky Lu
    • Miriam A. Guevara
      Miriam A. Guevara
      Department of Pathology, Microbiology and Immunology, Vanderbilt University Medical Center, Nashville, Tennessee 37212, United States
      More by Miriam A. Guevara
    • Ryan S. Doster
      Ryan S. Doster
      Department of Medicine, Vanderbilt University School of Medicine, Nashville, Tennessee 37212, United States
      More by Ryan S. Doster
    • Schuyler A. Chambers
      Schuyler A. Chambers
      Department of Chemistry, Vanderbilt University, Nashville, Tennessee 37235, United States
      More by Schuyler A. Chambers
      Orcidhttps://orcid.org/0000-0002-3557-830X
    • Lisa M. Rogers
      Lisa M. Rogers
      Department of Medicine, Vanderbilt University School of Medicine, Nashville, Tennessee 37212, United States
      More by Lisa M. Rogers
    • Rebecca E. Moore
      Rebecca E. Moore
      Department of Chemistry, Vanderbilt University, Nashville, Tennessee 37235, United States
      More by Rebecca E. Moore
    • Sabrina K. Spicer
      Sabrina K. Spicer
      Department of Chemistry, Vanderbilt University, Nashville, Tennessee 37235, United States
      More by Sabrina K. Spicer
    • Alison J. Eastman
      Alison J. Eastman
      Department of Medicine, Vanderbilt University School of Medicine, Nashville, Tennessee 37212, United States
      More by Alison J. Eastman
    • Jamisha D. Francis
      Jamisha D. Francis
      Department of Pathology, Microbiology and Immunology, Vanderbilt University Medical Center, Nashville, Tennessee 37212, United States
      More by Jamisha D. Francis
    • Shannon D. Manning
      Shannon D. Manning
      Department of Microbiology and Molecular Genetics, Michigan State University, East Lansing, Michigan 48823, United States
      More by Shannon D. Manning
    • Lakshmi Rajagopal
      Lakshmi Rajagopal
      Department of Pediatrics, University of Washington, Seattle, Washington 98109, United States
      More by Lakshmi Rajagopal
    • David M. Aronoff
      David M. Aronoff
      Department of Pathology, Microbiology and Immunology, Vanderbilt University Medical Center, Nashville, Tennessee 37212, United States
      Department of Medicine, Vanderbilt University School of Medicine, Nashville, Tennessee 37212, United States
      Departments of Biochemistry and Chemistry, Vanderbilt University, Nashville, Tennessee 37235, United States
      More by David M. Aronoff
    • Steven D. Townsend
      Steven D. Townsend
      Department of Chemistry, Vanderbilt University, Nashville, Tennessee 37235, United States
      More by Steven D. Townsend
      Orcidhttps://orcid.org/0000-0001-5362-7235
    • Jennifer A. Gaddy*
      Jennifer A. Gaddy
      Department of Pathology, Microbiology and Immunology, Vanderbilt University Medical Center, Nashville, Tennessee 37212, United States
      Department of Medicine, Vanderbilt University School of Medicine, Nashville, Tennessee 37212, United States
      Department of Veterans Affairs, Tennessee Valley Healthcare Systems, Nashville, Tennessee 37212, United States
      * Address correspondence to Jennifer A. Gaddy, Ph.D. Vanderbilt University School of Medicine- Division of Infectious Diseases A2200 Medical Center North 1161 21st Avenue South Nashville, Tennessee, U.S.A. 37232 Telephone: (615)-873-7884 Fax: (615) 343-6160[email protected]
      More by Jennifer A. Gaddy
      Orcidhttps://orcid.org/0000-0002-2192-4224
    Other Access OptionsSupporting Information (1)

    ACS Infectious Diseases

    Cite this: ACS Infect. Dis. 2021, 7, 9, 2686–2696
    Click to copy citationCitation copied!
    https://doi.org/10.1021/acsinfecdis.1c00182
    Published June 2, 2021
    Copyright © 2021 American Chemical Society
    Request reuse permissions

    Abstract

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    Abstract Image

    Group B Streptococcus (GBS) is an encapsulated Gram-positive pathogen that causes ascending infections of the reproductive tract during pregnancy. The capsule of this organism is a critical virulence factor that has been implicated in a variety of cellular processes to promote pathogenesis. Primarily comprised of carbohydrates, the GBS capsule and its synthesis is driven by the capsule polysaccharide synthesis (cps) operon. The cpsE gene within this operon encodes a putative glycosyltransferase that is responsible for the transfer of a Glc-1-P from UDP-Glc to an undecaprenyl lipid molecule. We hypothesized that the cpsE gene product is important for GBS virulence and ascending infection during pregnancy. Our work demonstrates that a GBS cpsE mutant secretes fewer carbohydrates, has a reduced capsule, and forms less biofilm than the wild-type parental strain. We show that, compared to the parental strain, the ΔcpsE deletion mutant is more readily taken up by human placental macrophages and has a significantly attenuated ability to invade and proliferate in the mouse reproductive tract. Taken together, these results demonstrate that the cpsE gene product is an important virulence factor that aids in GBS colonization and invasion of the gravid reproductive tract.

    Copyright © 2021 American Chemical Society

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    Supporting Information

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    Cited By

    Click to copy section linkSection link copied!

    This article is cited by 8 publications.

    1. Rebecca E. Moore, Sabrina K. Spicer, Jacky Lu, Schuyler A. Chambers, Kristen N. Noble, Jonathan Lochner, Rebecca C. Christofferson, Karla A. Vasco, Shannon D. Manning, Steven D. Townsend, Jennifer A. Gaddy. The Utility of Human Milk Oligosaccharides against Group B Streptococcus Infections of Reproductive Tissues and Cognate Adverse Pregnancy Outcomes. ACS Central Science 2023, 9 (9) , 1737-1749. https://doi.org/10.1021/acscentsci.3c00101
    2. Rebecca E. Moore, Sabrina K. Spicer, Julie A. Talbert, Shannon D. Manning, Steven D. Townsend, Jennifer A. Gaddy. Anti‐biofilm Activity of Human Milk Oligosaccharides in Clinical Strains of Streptococcus agalactiae with Diverse Capsular and Sequence Types. ChemBioChem 2023, 24 (6) https://doi.org/10.1002/cbic.202200643
    3. Jasmine Arya, Divya Sharma, Dev Kumar, Ritu Jakhar, Alka Khichi, Mehak Dangi, Anil Kumar Chhillar. Comparative genome analysis of Streptococcus strains to identify virulent genes causing neonatal meningitis. Infection, Genetics and Evolution 2023, 107 , 105398. https://doi.org/10.1016/j.meegid.2022.105398
    4. Jacky Lu, Rebecca E. Moore, Sabrina K. Spicer, Ryan S. Doster, Miriam A. Guevara, Jamisha D. Francis, Kristen N. Noble, Lisa M. Rogers, Julie A. Talbert, Michelle L. Korir, Steven D. Townsend, David M. Aronoff, Shannon D. Manning, Jennifer A. Gaddy, . Streptococcus agalactiae npx Is Required for Survival in Human Placental Macrophages and Full Virulence in a Model of Ascending Vaginal Infection during Pregnancy. mBio 2022, 13 (6) https://doi.org/10.1128/mbio.02870-22
    5. Yuxin Liu, Jinhui Liu. Group B Streptococcus: Virulence Factors and Pathogenic Mechanism. Microorganisms 2022, 10 (12) , 2483. https://doi.org/10.3390/microorganisms10122483
    6. Allison N Dammann, Anna B Chamby, Francisco J Gonzalez, Molly E Sharp, Karina Flores, Ifrah Shahi, Sophia Dongas, Thomas A Hooven, Adam J Ratner. Group B Streptococcus Capsular Serotype Alters Vaginal Colonization Fitness. The Journal of Infectious Diseases 2022, 225 (11) , 1896-1904. https://doi.org/10.1093/infdis/jiab559
    7. Min Liang, Wei Gong, Chongzhen Sun, Jielin Zhao, Hong Wang, Zonggang Chen, Min Xiao, Guofeng Gu. Sequential One‐Pot Three‐Enzyme Synthesis of the Tetrasaccharide Repeating Unit of Group B Streptococcus Serotype VIII Capsular Polysaccharide. Chinese Journal of Chemistry 2022, 40 (9) , 1039-1044. https://doi.org/10.1002/cjoc.202100822
    8. Jacky Lu, Miriam A. Guevara, Jamisha D. Francis, Sabrina K. Spicer, Rebecca E. Moore, Schuyler A. Chambers, Kelly M. Craft, Shannon D. Manning, Steven D. Townsend, Jennifer A. Gaddy. Analysis of Susceptibility to the Antimicrobial and Anti-Biofilm Activity of Human Milk Lactoferrin in Clinical Strains of Streptococcus agalactiae With Diverse Capsular and Sequence Types. Frontiers in Cellular and Infection Microbiology 2021, 11 https://doi.org/10.3389/fcimb.2021.740872
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    ACS Infectious Diseases

    Cite this: ACS Infect. Dis. 2021, 7, 9, 2686–2696
    Click to copy citationCitation copied!
    https://doi.org/10.1021/acsinfecdis.1c00182
    Published June 2, 2021
    Copyright © 2021 American Chemical Society
    Request reuse permissions

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