SARS-CoV-2 infectivity can be modulated through bacterial grooming of the glycocalyx
ABSTRACT The gastrointestinal (GI) tract is a site of replication of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) and GI symptoms are often reported by patients. SARS-CoV-2 cell entry depends upon heparan sulfate (HS) proteoglycans, which commensal bacteria that bathe the human mucos...
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American Society for Microbiology
2025-04-01
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| Online Access: | https://journals.asm.org/doi/10.1128/mbio.04015-24 |
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| author | Cameron Martino Benjamin P. Kellman Daniel R. Sandoval Thomas Mandel Clausen Robert Cooper Alhosna Benjdia Feryel Soualmia Alex E. Clark Aaron F. Garretson Clarisse A. Marotz Se Jin Song Stephen Wandro Livia S. Zaramela Rodolfo A. Salido Qiyun Zhu Erick Armingol Yoshiki Vázquez-Baeza Daniel McDonald James T. Sorrentino Bryn Taylor Pedro Belda-Ferre Promi Das Farhana Ali Chenguang Liang Yujie Zhang Luca Schifanella Alice Covizzi Alessia Lai Agostino Riva Christopher Basting Courtney Ann Broedlow Aki S. Havulinna Pekka Jousilahti Mehrbod Estaki Tomasz Kosciolek Rayus Kuplicki Teresa A. Victor Martin P. Paulus Kristen E. Savage Jennifer L. Benbow Emma S. Spielfogel Cheryl A. M. Anderson Maria Elena Martinez James V. Lacey Shi Huang Niina Haiminen Laxmi Parida Ho-Cheol Kim Jack A. Gilbert Daniel A. Sweeney Sarah M. Allard Austin D. Swafford Susan Cheng Michael Inouye Teemu Niiranen Mohit Jain Veikko Salomaa Karsten Zengler Nichole R. Klatt Jeff Hasty Olivier Berteau Aaron F. Carlin Jeffrey D. Esko Nathan E. Lewis Rob Knight |
| author_facet | Cameron Martino Benjamin P. Kellman Daniel R. Sandoval Thomas Mandel Clausen Robert Cooper Alhosna Benjdia Feryel Soualmia Alex E. Clark Aaron F. Garretson Clarisse A. Marotz Se Jin Song Stephen Wandro Livia S. Zaramela Rodolfo A. Salido Qiyun Zhu Erick Armingol Yoshiki Vázquez-Baeza Daniel McDonald James T. Sorrentino Bryn Taylor Pedro Belda-Ferre Promi Das Farhana Ali Chenguang Liang Yujie Zhang Luca Schifanella Alice Covizzi Alessia Lai Agostino Riva Christopher Basting Courtney Ann Broedlow Aki S. Havulinna Pekka Jousilahti Mehrbod Estaki Tomasz Kosciolek Rayus Kuplicki Teresa A. Victor Martin P. Paulus Kristen E. Savage Jennifer L. Benbow Emma S. Spielfogel Cheryl A. M. Anderson Maria Elena Martinez James V. Lacey Shi Huang Niina Haiminen Laxmi Parida Ho-Cheol Kim Jack A. Gilbert Daniel A. Sweeney Sarah M. Allard Austin D. Swafford Susan Cheng Michael Inouye Teemu Niiranen Mohit Jain Veikko Salomaa Karsten Zengler Nichole R. Klatt Jeff Hasty Olivier Berteau Aaron F. Carlin Jeffrey D. Esko Nathan E. Lewis Rob Knight |
| author_sort | Cameron Martino |
| collection | DOAJ |
| description | ABSTRACT The gastrointestinal (GI) tract is a site of replication of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) and GI symptoms are often reported by patients. SARS-CoV-2 cell entry depends upon heparan sulfate (HS) proteoglycans, which commensal bacteria that bathe the human mucosa are known to modify. To explore human gut HS-modifying bacterial abundances and how their presence may impact SARS-CoV-2 infection, we developed a task-based analysis of proteoglycan degradation on large-scale shotgun metagenomic data. We observed that gut bacteria with high predicted catabolic capacity for HS differ by age and sex, factors associated with coronavirus disease 2019 (COVID-19) severity, and directly by disease severity during/after infection, but do not vary between subjects with COVID-19 comorbidities or by diet. Gut commensal bacterial HS-modifying enzymes reduce spike protein binding and infection of authentic SARS-CoV-2, suggesting that bacterial grooming of the GI mucosa may impact viral susceptibility.IMPORTANCESevere acute respiratory syndrome coronavirus 2 (SARS-CoV-2), the virus responsible for coronavirus disease 2019, can infect the gastrointestinal (GI) tract, and individuals who exhibit GI symptoms often have more severe disease. The GI tract’s glycocalyx, a component of the mucosa covering the large intestine, plays a key role in viral entry by binding SARS-CoV-2’s spike protein via heparan sulfate (HS). Here, using metabolic task analysis of multiple large microbiome sequencing data sets of the human gut microbiome, we identify a key commensal human intestinal bacteria capable of grooming glycocalyx HS and modulating SARS-CoV-2 infectivity in vitro. Moreover, we engineered the common probiotic Escherichia coli Nissle 1917 (EcN) to effectively block SARS-CoV-2 binding and infection of human cell cultures. Understanding these microbial interactions could lead to better risk assessments and novel therapies targeting viral entry mechanisms. |
| format | Article |
| id | doaj-art-f8933efd76b74a03a865e37d15ee0fb9 |
| institution | DOAJ |
| issn | 2150-7511 |
| language | English |
| publishDate | 2025-04-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | mBio |
| spelling | doaj-art-f8933efd76b74a03a865e37d15ee0fb92025-08-20T03:17:58ZengAmerican Society for MicrobiologymBio2150-75112025-04-0116410.1128/mbio.04015-24SARS-CoV-2 infectivity can be modulated through bacterial grooming of the glycocalyxCameron Martino0Benjamin P. Kellman1Daniel R. Sandoval2Thomas Mandel Clausen3Robert Cooper4Alhosna Benjdia5Feryel Soualmia6Alex E. Clark7Aaron F. Garretson8Clarisse A. Marotz9Se Jin Song10Stephen Wandro11Livia S. Zaramela12Rodolfo A. Salido13Qiyun Zhu14Erick Armingol15Yoshiki Vázquez-Baeza16Daniel McDonald17James T. Sorrentino18Bryn Taylor19Pedro Belda-Ferre20Promi Das21Farhana Ali22Chenguang Liang23Yujie Zhang24Luca Schifanella25Alice Covizzi26Alessia Lai27Agostino Riva28Christopher Basting29Courtney Ann Broedlow30Aki S. Havulinna31Pekka Jousilahti32Mehrbod Estaki33Tomasz Kosciolek34Rayus Kuplicki35Teresa A. Victor36Martin P. Paulus37Kristen E. Savage38Jennifer L. Benbow39Emma S. Spielfogel40Cheryl A. M. Anderson41Maria Elena Martinez42James V. Lacey43Shi Huang44Niina Haiminen45Laxmi Parida46Ho-Cheol Kim47Jack A. Gilbert48Daniel A. Sweeney49Sarah M. Allard50Austin D. Swafford51Susan Cheng52Michael Inouye53Teemu Niiranen54Mohit Jain55Veikko Salomaa56Karsten Zengler57Nichole R. Klatt58Jeff Hasty59Olivier Berteau60Aaron F. Carlin61Jeffrey D. Esko62Nathan E. Lewis63Rob Knight64Department of Pediatrics, University of California San Diego School of Medicine, La Jolla, California, USADepartment of Pediatrics, University of California San Diego School of Medicine, La Jolla, California, USADepartment of Cellular and Molecular Medicine, University of California San Diego, La Jolla, California, USADepartment of Cellular and Molecular Medicine, University of California San Diego, La Jolla, California, USADepartment of Bioengineering, University of California San Diego, La Jolla, California, USAUniversité Paris-Saclay, INRAE, AgroParisTech, Micalis Institute, ChemSyBio, 78350, Jouy-en-Josas, FranceUniversité Paris-Saclay, INRAE, AgroParisTech, Micalis Institute, ChemSyBio, 78350, Jouy-en-Josas, FranceDepartment of Medicine, University of California San Diego, La Jolla, California, USADepartment of Medicine, University of California San Diego, La Jolla, California, USADepartment of Pediatrics, University of California San Diego School of Medicine, La Jolla, California, USACenter for Microbiome Innovation, University of California San Diego, La Jolla, California, USACenter for Microbiome Innovation, University of California San Diego, La Jolla, California, USADepartment of Pediatrics, University of California San Diego School of Medicine, La Jolla, California, USADepartment of Pediatrics, University of California San Diego School of Medicine, La Jolla, California, USADepartment of Pediatrics, University of California San Diego School of Medicine, La Jolla, California, USADepartment of Pediatrics, University of California San Diego School of Medicine, La Jolla, California, USACenter for Microbiome Innovation, University of California San Diego, La Jolla, California, USADepartment of Pediatrics, University of California San Diego School of Medicine, La Jolla, California, USADepartment of Pediatrics, University of California San Diego School of Medicine, La Jolla, California, USABiomedical Sciences Graduate Program, University of California San Diego, La Jolla, California, USADepartment of Pediatrics, University of California San Diego School of Medicine, La Jolla, California, USADepartment of Pediatrics, University of California San Diego School of Medicine, La Jolla, California, USADepartment of Pediatrics, University of California San Diego School of Medicine, La Jolla, California, USADepartment of Pediatrics, University of California San Diego School of Medicine, La Jolla, California, USADepartment of Bioengineering, University of California San Diego, La Jolla, California, USADepartment of Surgery, Division of Surgical Outcomes and Precision Medicine Research, Medical School, University of Minnesota, Minneapolis, Minnesota, USADepartment of Infectious diseases, Luigi Sacco Hospital, Milan and Department of Biomedical and Clinical Sciences (DIBIC), University of Milan, Milan, ItalyDepartment of Infectious diseases, Luigi Sacco Hospital, Milan and Department of Biomedical and Clinical Sciences (DIBIC), University of Milan, Milan, ItalyDepartment of Infectious diseases, Luigi Sacco Hospital, Milan and Department of Biomedical and Clinical Sciences (DIBIC), University of Milan, Milan, ItalyDepartment of Surgery, Division of Surgical Outcomes and Precision Medicine Research, Medical School, University of Minnesota, Minneapolis, Minnesota, USADepartment of Surgery, Division of Surgical Outcomes and Precision Medicine Research, Medical School, University of Minnesota, Minneapolis, Minnesota, USADepartment of Public Health and Welfare, Finnish Institute for Health and Welfare, Helsinki and Turku, FinlandDepartment of Public Health and Welfare, Finnish Institute for Health and Welfare, Helsinki and Turku, FinlandDepartment of Pediatrics, University of California San Diego School of Medicine, La Jolla, California, USADepartment of Pediatrics, University of California San Diego School of Medicine, La Jolla, California, USALaureate Institute for Brain Research, Tulsa, Oklahoma, USALaureate Institute for Brain Research, Tulsa, Oklahoma, USALaureate Institute for Brain Research, Tulsa, Oklahoma, USADivision of Health Analytics, Department of Computational and Quantitative Medicine, City of Hope, Duarte, California, USADivision of Health Analytics, Department of Computational and Quantitative Medicine, City of Hope, Duarte, California, USADivision of Health Analytics, Department of Computational and Quantitative Medicine, City of Hope, Duarte, California, USAHerbert Wertheim School of Public Health and Human Longevity Science, University of California San Diego, La Jolla, California, USAHerbert Wertheim School of Public Health and Human Longevity Science, University of California San Diego, La Jolla, California, USADivision of Health Analytics, Department of Computational and Quantitative Medicine, City of Hope, Duarte, California, USADepartment of Pediatrics, University of California San Diego School of Medicine, La Jolla, California, USAIBM T. J. Watson Research Center, Yorktown Heights, New York, USAIBM T. J. Watson Research Center, Yorktown Heights, New York, USAAI and Cognitive Software, IBM Research-Almaden, San Jose, California, USADepartment of Pediatrics, University of California San Diego School of Medicine, La Jolla, California, USADivision of Pulmonary, Critical Care and Sleep Medicine, Department of Medicine, University of California San Diego, La Jolla, California, USADepartment of Pediatrics, University of California San Diego School of Medicine, La Jolla, California, USACenter for Microbiome Innovation, University of California San Diego, La Jolla, California, USADivision of Cardiology, Brigham and Women’s Hospital, Boston, Massachusetts, USAHealth Data Research UK Cambridge, Wellcome Genome Campus and University of Cambridge, Cambridge, United KingdomDepartment of Public Health and Welfare, Finnish Institute for Health and Welfare, Helsinki and Turku, FinlandDepartment of Pharmacology, University of California, San Diego, La Jolla, California, USADepartment of Public Health and Welfare, Finnish Institute for Health and Welfare, Helsinki and Turku, FinlandDepartment of Pediatrics, University of California San Diego School of Medicine, La Jolla, California, USADepartment of Surgery, Division of Surgical Outcomes and Precision Medicine Research, Medical School, University of Minnesota, Minneapolis, Minnesota, USADepartment of Bioengineering, University of California San Diego, La Jolla, California, USAUniversité Paris-Saclay, INRAE, AgroParisTech, Micalis Institute, ChemSyBio, 78350, Jouy-en-Josas, FranceDepartment of Medicine, University of California San Diego, La Jolla, California, USADepartment of Cellular and Molecular Medicine, University of California San Diego, La Jolla, California, USADepartment of Pediatrics, University of California San Diego School of Medicine, La Jolla, California, USADepartment of Pediatrics, University of California San Diego School of Medicine, La Jolla, California, USAABSTRACT The gastrointestinal (GI) tract is a site of replication of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) and GI symptoms are often reported by patients. SARS-CoV-2 cell entry depends upon heparan sulfate (HS) proteoglycans, which commensal bacteria that bathe the human mucosa are known to modify. To explore human gut HS-modifying bacterial abundances and how their presence may impact SARS-CoV-2 infection, we developed a task-based analysis of proteoglycan degradation on large-scale shotgun metagenomic data. We observed that gut bacteria with high predicted catabolic capacity for HS differ by age and sex, factors associated with coronavirus disease 2019 (COVID-19) severity, and directly by disease severity during/after infection, but do not vary between subjects with COVID-19 comorbidities or by diet. Gut commensal bacterial HS-modifying enzymes reduce spike protein binding and infection of authentic SARS-CoV-2, suggesting that bacterial grooming of the GI mucosa may impact viral susceptibility.IMPORTANCESevere acute respiratory syndrome coronavirus 2 (SARS-CoV-2), the virus responsible for coronavirus disease 2019, can infect the gastrointestinal (GI) tract, and individuals who exhibit GI symptoms often have more severe disease. The GI tract’s glycocalyx, a component of the mucosa covering the large intestine, plays a key role in viral entry by binding SARS-CoV-2’s spike protein via heparan sulfate (HS). Here, using metabolic task analysis of multiple large microbiome sequencing data sets of the human gut microbiome, we identify a key commensal human intestinal bacteria capable of grooming glycocalyx HS and modulating SARS-CoV-2 infectivity in vitro. Moreover, we engineered the common probiotic Escherichia coli Nissle 1917 (EcN) to effectively block SARS-CoV-2 binding and infection of human cell cultures. Understanding these microbial interactions could lead to better risk assessments and novel therapies targeting viral entry mechanisms.https://journals.asm.org/doi/10.1128/mbio.04015-24SARS-CoV-2Covidhuman microbiomeagingHeparan Sulfate |
| spellingShingle | Cameron Martino Benjamin P. Kellman Daniel R. Sandoval Thomas Mandel Clausen Robert Cooper Alhosna Benjdia Feryel Soualmia Alex E. Clark Aaron F. Garretson Clarisse A. Marotz Se Jin Song Stephen Wandro Livia S. Zaramela Rodolfo A. Salido Qiyun Zhu Erick Armingol Yoshiki Vázquez-Baeza Daniel McDonald James T. Sorrentino Bryn Taylor Pedro Belda-Ferre Promi Das Farhana Ali Chenguang Liang Yujie Zhang Luca Schifanella Alice Covizzi Alessia Lai Agostino Riva Christopher Basting Courtney Ann Broedlow Aki S. Havulinna Pekka Jousilahti Mehrbod Estaki Tomasz Kosciolek Rayus Kuplicki Teresa A. Victor Martin P. Paulus Kristen E. Savage Jennifer L. Benbow Emma S. Spielfogel Cheryl A. M. Anderson Maria Elena Martinez James V. Lacey Shi Huang Niina Haiminen Laxmi Parida Ho-Cheol Kim Jack A. Gilbert Daniel A. Sweeney Sarah M. Allard Austin D. Swafford Susan Cheng Michael Inouye Teemu Niiranen Mohit Jain Veikko Salomaa Karsten Zengler Nichole R. Klatt Jeff Hasty Olivier Berteau Aaron F. Carlin Jeffrey D. Esko Nathan E. Lewis Rob Knight SARS-CoV-2 infectivity can be modulated through bacterial grooming of the glycocalyx mBio SARS-CoV-2 Covid human microbiome aging Heparan Sulfate |
| title | SARS-CoV-2 infectivity can be modulated through bacterial grooming of the glycocalyx |
| title_full | SARS-CoV-2 infectivity can be modulated through bacterial grooming of the glycocalyx |
| title_fullStr | SARS-CoV-2 infectivity can be modulated through bacterial grooming of the glycocalyx |
| title_full_unstemmed | SARS-CoV-2 infectivity can be modulated through bacterial grooming of the glycocalyx |
| title_short | SARS-CoV-2 infectivity can be modulated through bacterial grooming of the glycocalyx |
| title_sort | sars cov 2 infectivity can be modulated through bacterial grooming of the glycocalyx |
| topic | SARS-CoV-2 Covid human microbiome aging Heparan Sulfate |
| url | https://journals.asm.org/doi/10.1128/mbio.04015-24 |
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