SARS-CoV-2 infectivity can be modulated through bacterial grooming of the glycocalyx
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 Jr, 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
mBio, doi:10.1128/mbio.04015-24
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. IMPORTANCE Severe 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.
AUTHOR AFFILIATIONS
ADDITIONAL FILES The following material is available online.
Supplemental Material Supplemental Material (mBio04015-24-s0001.pdf). Supplemental figures and tables.
References
Bankevich, Nurk, Antipov, Gurevich, Dvorkin et al., SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing, J Comput Biol,
doi:10.1089/cmb.2012.0021Beck, Schloss, Venkataraman, Twigg H 3rd, Jablonski et al., Multicenter comparison of lung and oral microbiomes of HIVinfected and HIV-uninfected Individuals, Am J Respir Crit Care Med,
doi:10.1164/rccm.202008-3146EDBelda-Ferre, Knight, Nathan, National Institutes of Health (NIH) 1P30DK120515, Lewis HHS | National Institutes of Health (NIH) R
Benjdia, Leprince, Sandström, Vaudry, Berteau, Mechanistic investigations of anaerobic sulfatase-maturating enzyme: direct Cbeta H-atom abstraction catalyzed by a radical AdoMet enzyme, J Am Chem Soc,
doi:10.1021/ja901571pBenjdia, Martens, Gordon, Berteau, Sulfatases and a radical S-adenosyl-L-methionine (AdoMet) enzyme are key for mucosal foraging and fitness of the prominent human gut symbiont, Bacteroides thetaiotaomicron, J Biol Chem,
doi:10.3389/fnut.2022.934568Borodulin, Tolonen, Jousilahti, Jula, Juolevi et al., Cohort profile: the national FINRISK study, Int J Epidemiol,
doi:10.3389/fnut.2022.934568Brownlee, Havler, Dettmar, Allen, Pearson, Colonic mucus: secretion and turnover in relation to dietary fibre intake, Proc Nutr Soc,
doi:10.1079/pns2003206Budden, Gellatly, Wood, Cooper, Morrison et al., Emerging pathogenic links between microbiota and the gut-lung axis, Nat Rev Microbiol,
doi:10.1038/nrmicro.2016.142Cagno, Tseligka, Jones, Tapparel, Heparan sulfate proteoglycans and viral attachment: true receptors or adaptation bias?, Viruses,
doi:10.1038/nature18847Cartmell, Lowe, Baslé, Firbank, Ndeh et al., How members of the human gut microbiota overcome the sulfation problem posed by glycosaminoglycans, Proc Natl Acad Sci U S A,
doi:10.1073/pnas.1704367114Cheung, Goh, Lim, Tien, Lim et al., Residual SARS-CoV-2 viral antigens detected in GI and hepatic tissues from five recovered patients with COVID-19, Gut,
doi:10.1136/gutjnl-2021-324280Chu, Chan, Wang, Yuen, Chai et al., SARS-Cov-2 induces a more robust innate immune response and replicates less efficiently than SARS-CoV in the human intestines: an ex vivo study with implications on pathogenesis of COVID-19, Cell Mol Gastroenterol Hepatol,
doi:10.1136/gutjnl-2021-324280Clausen, Sandoval, Spliid, Pihl, Perrett et al., SARS-CoV-2 infection depends on cellular heparan sulfate and ACE2, Cell,
doi:10.1016/j.sbi.2022.102439De La Cuesta-Zuluaga, Kelley, Chen, Escobar, Mueller et al., Ageand sex-dependent patterns of gut microbial diversity in human adults, mSystems,
doi:10.3389/fnut.2022.934568Desai, Seekatz, Koropatkin, Kamada, Hickey et al., A dietary fiberdeprived gut microbiota degrades the colonic mucus barrier and enhances pathogen susceptibility, Cell,
doi:10.3389/fnut.2022.934568Earle, Billings, Sigal, Lichtman, Hansson et al., Quantitative imaging of gut microbiota spatial organization, Cell Host Microbe,
doi:10.3389/fnut.2022.934568Eilam, Zarecki, Oberhardt, Ursell, Kupiec et al., Glycan degradation (GlyDeR) analysis predicts mammalian gut microbiota abundance and host diet-specific adaptations, MBio,
doi:10.1128/mBio.01526-14Elena, James, Lacey, None
Elshazli, Kline, Elgaml, Aboutaleb, Salim et al., Gastroenterology manifestations and COVID-19 outcomes: a meta-analysis of 25,252 cohorts among the first and second waves, J Med Virol,
doi:10.1136/gutjnl-2021-324280Grondin, Tamura, Déjean, Abbott, Brumer, Polysaccharide utilization loci: fueling microbial communities, J Bacteriol,
doi:10.1128/JB.00860-16Guo, Tao, Flavell, Zhu, Potential intestinal infection and faecal-oral transmission of SARS-CoV-2, Nat Rev Gastroenterol Hepatol,
doi:10.1136/gutjnl-2021-324280Han, Duan, Yang, Nilsson-Payant, Wang et al., Identification of SARS-CoV-2 inhibitors using lung and colonic organoids, Nature New Biol,
doi:10.1038/s41586-020-2901-9Hayashi, Wagatsuma, Nojima, Yamakawa, Ichimiya et al., The characteristics of gastrointestinal symptoms in patients with severe COVID-19: a systematic review and meta-analysis, J Gastroenterol,
doi:10.1136/gutjnl-2021-324280Hedemann, Theil, Knudsen, The thickness of the intestinal mucous layer in the colon of rats fed various sources of nondigestible carbohydrates is positively correlated with the pool of SCFA but negatively correlated with the proportion of butyric acid in digesta, Br J Nutr,
doi:10.1017/S0007114508143549Hillmann, Al-Ghalith, Shields-Cutler, Zhu, Gohl et al., Evaluating the information content of shallow shotgun metagenomics, mSystems,
doi:10.1093/bioinformatics/btu170Hobbs, Pluvinage, Boraston, Glycan-metabolizing enzymes in microbe-host interactions: the Streptococcus pneumoniae paradigm, FEBS Lett,
doi:10.1002/1873-3468.13045Inoyue, None
Jeffrey, Alfred Benzon Foundation, The Alfred Benzon Foundation) Thomas Mandel Clausen Academy of Finland 321351 and 354447 Teemu Niiranen Emil Aaltosen Säätiö
Jennifer, Benbow, Spielfogel Cheryl, Anderson Maria, James, None
Jennifer, Benbow, Spielfogel Cheryl, Anderson, Elena et al., National Institutes of Health (NIH)
Jennifer, Benbow, Spielfogel Cheryl, Anderson, Elena et al., National Institutes of Health (NIH) P
Jennifer, Benbow, Spielfogel Cheryl, Anderson, Elena et al., National Institutes of Health (NIH) P
Jennifer, Benbow, Spielfogel Cheryl, Anderson, None, Research Article mBio
Jin, Ananthanarayanan, Brown, Rager, Bram et al., SARS CoV-2 detected in neonatal stool remote from maternal COVID-19 during pregnancy, Pediatr Res,
doi:10.1136/gutjnl-2021-324280Johansson, Phillipson, Petersson, Velcich, Holm et al., The inner of the two Muc2 mucin-dependent mucus layers in colon is devoid of bacteria, Proc Natl Acad Sci U S A,
doi:10.1073/pnas.0803124105Kanehisa, Furumichi, Tanabe, Sato, Morishima, KEGG: new perspectives on genomes, pathways, diseases and drugs, Nucleic Acids Res,
doi:10.1093/nar/gkw1092Kearns, Sandoval, Casalino, Clausen, Rosenfeld et al., Spike-heparan sulfate interactions in SARS-CoV-2 infection, Curr Opin Struct Biol,
doi:10.1016/j.sbi.2022.102439Koropatkin, Cameron, Martens, How glycan metabolism shapes the human gut microbiota, Nat Rev Microbiol,
doi:10.1038/nrmicro2746Lagesen, Hallin, Rødland, Staerfeldt, Rognes et al., RNAmmer: consistent and rapid annotation of ribosomal RNA genes, Nucleic Acids Res,
doi:10.1093/bioinformatics/btu170Langdon, Performance of genetic programming optimised Bowtie2 on genome comparison and analytic testing (GCAT) bench marks, BioData Min,
doi:10.1186/s13040-014-0034-0Lee, Kim, Park, OrthoANI: an improved algorithm and software for calculating average nucleotide identity, Int J Syst Evol Microbiol,
doi:10.1099/ijsem.0.000760Lewis, None
Lloyd-Price, Mahurkar, Rahnavard, Crabtree, Orvis et al., Erratum: strains, functions and dynamics in the expanded human microbiome project, Nature New Biol,
doi:10.1038/nature24485Lombard, Ramulu, Drula, Coutinho, Henrissat, The carbohydrate-active enzymes database (CAZy) in 2013, Nucleic Acids Res,
doi:10.1093/nar/gkt1178Machado, Andrejev, Tramontano, Patil, Fast automated reconstruction of genome-scale metabolic models for microbial species and communities, Nucleic Acids Res,
doi:10.1093/nar/gky537Magnúsdóttir, Heinken, Kutt, Ravcheev, Bauer et al., Generation of genome-scale metabolic reconstructions for 773 members of the human gut microbiota, Nat Biotechnol,
doi:10.1038/nbt.3703Marotz, Belda-Ferre, Ali, Das, Huang et al., SARS-CoV-2 detection status associates with bacterial community composition in patients and the hospital environment, Microbiome,
doi:10.3389/fnut.2022.934568Marotz, Salido, Zhu, Mcdonald, Taylor et al., None
Martino, Dilmore, Burcham, Metcalf, Jeste et al., Microbiota succession throughout life from the cradle to the grave, Nat Rev Microbiol,
doi:10.1164/rccm.202008-3146EDMcdonald, Hyde, Debelius, Morton, Gonzalez et al., American gut: an open platform for citizen science microbiome research, mSystems,
doi:10.1038/nature18847Mcdonald, Knight, University of California
Mehta, Mcauley, Brown, Sanchez, Tattersall et al., COVID-19: consider cytokine storm syndromes and immunosuppression, Lancet,
doi:10.1136/gutjnl-2021-324280Natarajan, Zlitni, Brooks, Vance, Dahlen et al., Gastrointestinal symptoms and fecal shedding of SARS-CoV-2 RNA suggest prolonged gastrointestinal infection, Med,
doi:10.1136/gutjnl-2021-324280Ndeh, Baslé, Strahl, Yates, Mcclurgg et al., Metabolism of multiple glycosaminoglycans by Bacteroides thetaiotaomicron is orchestrated by a versatile core genetic locus, Nat Commun,
doi:10.1038/s41467-020-14509-4Pruitt, Tatusova, Maglott, NCBI reference sequences (RefSeq): a curated non-redundant sequence database of genomes, transcripts and proteins, Nucleic Acids Res,
doi:10.1093/bioinformatics/btu170Redd, Zhou, Hathorn, Mccarty, Bazarbashi et al., Prevalence and characteristics of gastroin testinal symptoms in patients with severe acute respiratory syndrome coronavirus 2 infection in the united states: a multicenter cohort study, Gastroenterology,
doi:10.3389/fnut.2022.934568Reed, Famili, Thiele, Palsson, Towards multidimensional genome annotation, Nat Rev Genet,
doi:10.1038/nrg1769Richelle, Chiang, Kuo, Ne, Increasing consensus of context-specific metabolic models by integrating data-inferred cell functions, PLoS Comput Biol,
doi:10.1093/bioinformatics/btu170Richelle, Kellman, Wenzel, Chiang, Reagan et al., Model-based assessment of mammalian cell metabolic functionalities using omics data, Cell Rep Methods,
doi:10.3389/fnut.2022.934568Robb, Hobbs, Woodiga, Shapiro-Ward, Suits et al., Molecular characteri zation of N-glycan degradation and transport in Streptococcus pneumoniae and its contribution to virulence, PLoS Pathog,
doi:10.1371/journal.ppat.1006090Salomaa, National Institutes of Health (NIH) R01ES027595 Mohit Jain ANID Becas Chile Doctorado, Erick Armingol Research Article mBio
Salosensaari, Laitinen, Havulinna, Meric, Cheng et al., Taxonomic signatures of long-term mortality risk in human gut microbiota, Epidemiology,
doi:10.3389/fnut.2022.934568Sanders, Nurk, Salido, Minich, Xu et al., Optimizing sequencing protocols for leaderboard metagenomics by combining long and short reads, Genome Biol,
doi:10.1186/s13059-019-1834-9Ulmer, Vilén, Namburi, Benjdia, Beneteau et al., Characterization of glycosaminoglycan (GAG) sulfatases from the human gut symbiont bacteroides thetaiotaomicron reveals the first GAG-specific bacterial endosulfatase, J Biol Chem,
doi:10.1074/jbc.M114.573303Vajargah, Zargarzadeh, Ebrahimzadeh, Mousavi, Mobasheran et al., Association of fruits, vegetables, and fiber intake with COVID-19 severity and symptoms in hospitalized patients: a cross-sectional study, Front Nutr,
doi:10.3389/fnut.2022.934568Vespa, Pugliese, Colapietro, Aghemo, Stay (GI) Healthy: COVID-19 and gastrointestinal manifestations, Tech Innov Gastrointest Endosc,
doi:10.1136/gutjnl-2021-324280Weiss, Esko, Tor, Targeting heparin and heparan sulfate protein interactions, Org Biomol Chem,
doi:10.1039/C7OB01058CWilliamson, Walker, Bhaskaran, Bacon, Bates et al., OpenSAFELY: factors associated with COVID-19 death in 17 million patients, Nature New Biol,
doi:10.3389/fnut.2022.934568Woo, Shafiq, Fitzek, Dottermusch, Altmeppen et al., Vagus nerve inflammation contributes to dysautonomia in COVID-19, Acta Neuropathol,
doi:10.1136/gutjnl-2021-324280Yin, Mao, Yang, Chen, Mao et al., dbCAN: a web resource for automated carbohydrate-active enzyme annotation, Nucleic Acids Res,
doi:10.1093/nar/gks479Zaramela, Martino, Alisson-Silva, Rees, Diaz et al., Gut bacteria responding to dietary change encode sialidases that exhibit preference for red meat-associated carbohydrates, Nat Microbiol,
doi:10.3389/fnut.2022.934568Zhang, Kang, Gong, Xu, Wang et al., Digestive system is a potential route of COVID-19: an analysis of single-cell coexpression pattern of key proteins in viral entry process, Gut,
doi:10.1136/gutjnl-2020-320953Zhang, Yohe, Huang, Entwistle, Wu et al., dbCAN2: a meta server for automated carbohydrate-active enzyme annotation, Nucleic Acids Res,
doi:10.1093/nar/gky418Zhu, Mai, Pfeiffer, Janssen, Asnicar et al., Phylogenomics of 10,575 genomes reveals evolutionary proximity between domains bacteria and archaea, Nat Commun,
doi:10.3389/fnut.2022.934568Zhu, Vázquez, Shi, Niina, Laxmi et al., None, National Institutes of Health (NIH) P
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"abstract": "<jats:title>ABSTRACT</jats:title>\n <jats:sec>\n <jats:title/>\n <jats:p>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.</jats:p>\n <jats:sec>\n <jats:title>IMPORTANCE</jats:title>\n <jats:p>\n Severe 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\n <jats:italic>in vitro</jats:italic>\n . Moreover, we engineered the common probiotic\n <jats:italic>Escherichia coli</jats:italic>\n 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.\n </jats:p>\n </jats:sec>\n </jats:sec>",
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