Attach Me If You Can: Murine Norovirus Binds to Commensal Bacteria and Fungi

Overview

Journal Viruses

Publisher MDPI

Specialty Microbiology

Date 2020 Jul 18

PMID 32674489

Citations 15

Authors

Jasmine L Madrigal

Sutonuka Bhar

Samantha Hackett

Haley Engelken

Ross Joseph

Nemat O Keyhani

Melissa K Jones

Affiliations

Soon will be listed here.

Abstract

The presence of commensal bacteria enhances both acute and persistent infection of murine noroviruses. For several enteric viral pathogens, mechanisms by which these bacteria enhance infection involve direct interactions between the virus and bacteria. While it has been demonstrated that human noroviruses bind to a variety of commensal bacteria, it is not known if this is also true for murine noroviruses. The goal of this study was to characterize interactions between murine noroviruses and commensal bacteria and determine the impact of bacterial growth conditions, incubation temperature and time, on murine norovirus attachment to microbes that comprise the mammalian microbiome. We show that murine noroviruses bind directly to commensal bacteria and show similar patterns of attachment as human norovirus VLPs examined under the same conditions. Furthermore, while binding levels are not impacted by the growth phase of the bacteria, they do change with time and incubation temperature. We also found that murine norovirus can bind to a commensal fungal species, .

Citing Articles

Virus Association with Bacteria and Bacterial Cell Components Enhance Virus Infectivity.

Deng W, Almeida G, Gibson K Food Environ Virol. 2025; 17(1):15.

PMID: 39789292 PMC: 11717783. DOI: 10.1007/s12560-025-09633-7.

Changes in the Murine Microbiome and Bacterial Extracellular Vesicle Production in Response to Antibiotic Treatment and Norovirus Infection.

Mosby C, Long K, Phillips M, Bartel J, Jones M Viruses. 2023; 15(12).

PMID: 38140684 PMC: 10747002. DOI: 10.3390/v15122443.

Viral-Bacterial Interactions That Impact Viral Thermostability and Transmission.

Gonzalez L, Tat R, Greaves J, Robinson C Viruses. 2023; 15(12).

PMID: 38140656 PMC: 10747402. DOI: 10.3390/v15122415.

Therapeutic Approach Targeting Gut Microbiome in Gastrointestinal Infectious Diseases.

Han Z, Min Y, Pang K, Wu D Int J Mol Sci. 2023; 24(21).

PMID: 37958637 PMC: 10650060. DOI: 10.3390/ijms242115654.

Protective Effect of Select Bacterial Species Representative of Fresh Produce on Human Norovirus Surrogates Exposed to Disinfecting Pulsed Light.

Peloquin L, Goetz C, Jubinville E, Jean J Appl Environ Microbiol. 2023; 89(5):e0004323.

PMID: 37154750 PMC: 10231187. DOI: 10.1128/aem.00043-23.

References

Nash A, Auchtung T, Wong M, Smith D, Gesell J, Ross M . The gut mycobiome of the Human Microbiome Project healthy cohort. Microbiome. 2017; 5(1):153. PMC: 5702186. DOI: 10.1186/s40168-017-0373-4. View

Taube S, Perry J, Yetming K, Patel S, Auble H, Shu L . Ganglioside-linked terminal sialic acid moieties on murine macrophages function as attachment receptors for murine noroviruses. J Virol. 2009; 83(9):4092-101. PMC: 2668497. DOI: 10.1128/JVI.02245-08. View

Schwartz S, Vergoulidou M, Schreier E, Loddenkemper C, Reinwald M, Schmidt-Hieber M . Norovirus gastroenteritis causes severe and lethal complications after chemotherapy and hematopoietic stem cell transplantation. Blood. 2011; 117(22):5850-6. PMC: 7022229. DOI: 10.1182/blood-2010-12-325886. View

Neville B, dEnfert C, Bougnoux M . Candida albicans commensalism in the gastrointestinal tract. FEMS Yeast Res. 2015; 15(7). DOI: 10.1093/femsyr/fov081. View

Madrigal J, Jones M . Quantifying Human Norovirus Virus-like Particles Binding to Commensal Bacteria Using Flow Cytometry. J Vis Exp. 2020; (158). DOI: 10.3791/61048. View

Hernandez-Santos N, Klein B . Through the Scope Darkly: The Gut Mycobiome Comes into Focus. Cell Host Microbe. 2017; 22(6):728-729. PMC: 5964996. DOI: 10.1016/j.chom.2017.11.013. View

Ettayebi K, Crawford S, Murakami K, Broughman J, Karandikar U, Tenge V . Replication of human noroviruses in stem cell-derived human enteroids. Science. 2016; 353(6306):1387-1393. PMC: 5305121. DOI: 10.1126/science.aaf5211. View

Almand E, Moore M, Outlaw J, Jaykus L . Human norovirus binding to select bacteria representative of the human gut microbiota. PLoS One. 2017; 12(3):e0173124. PMC: 5336261. DOI: 10.1371/journal.pone.0173124. View

Almand E, Moore M, Jaykus L . Characterization of human norovirus binding to gut-associated bacterial ligands. BMC Res Notes. 2019; 12(1):607. PMC: 6755701. DOI: 10.1186/s13104-019-4669-2. View

10.

Grau K, Zhu S, Peterson S, Helm E, Philip D, Phillips M . The intestinal regionalization of acute norovirus infection is regulated by the microbiota via bile acid-mediated priming of type III interferon. Nat Microbiol. 2019; 5(1):84-92. PMC: 6925324. DOI: 10.1038/s41564-019-0602-7. View

11.

Erickson A, Jesudhasan P, Mayer M, Narbad A, Winter S, Pfeiffer J . Bacteria Facilitate Enteric Virus Co-infection of Mammalian Cells and Promote Genetic Recombination. Cell Host Microbe. 2018; 23(1):77-88.e5. PMC: 5764776. DOI: 10.1016/j.chom.2017.11.007. View

12.

Gow N, Yadav B . Microbe Profile: Candida albicans: a shape-changing, opportunistic pathogenic fungus of humans. Microbiology (Reading). 2017; 163(8):1145-1147. DOI: 10.1099/mic.0.000499. View

13.

Deng W, Almeida G, Gibson K . Co-culture with Enterobacter cloacae does not Enhance Virus Resistance to Thermal and Chemical Treatments. Food Environ Virol. 2019; 11(3):238-246. DOI: 10.1007/s12560-019-09381-5. View

14.

Li D, Breiman A, Le Pendu J, Uyttendaele M . Binding to histo-blood group antigen-expressing bacteria protects human norovirus from acute heat stress. Front Microbiol. 2015; 6:659. PMC: 4486850. DOI: 10.3389/fmicb.2015.00659. View

15.

Laforest-Lapointe I, Arrieta M . Microbial Eukaryotes: a Missing Link in Gut Microbiome Studies. mSystems. 2018; 3(2). PMC: 5850078. DOI: 10.1128/mSystems.00201-17. View

16.

Lei S, Samuel H, Twitchell E, Bui T, Ramesh A, Wen K . Enterobacter cloacae inhibits human norovirus infectivity in gnotobiotic pigs. Sci Rep. 2016; 6:25017. PMC: 4845002. DOI: 10.1038/srep25017. View

17.

Croxen M, Law R, Scholz R, Keeney K, Wlodarska M, Finlay B . Recent advances in understanding enteric pathogenic Escherichia coli. Clin Microbiol Rev. 2013; 26(4):822-80. PMC: 3811233. DOI: 10.1128/CMR.00022-13. View

18.

Kuss S, Best G, Etheredge C, Pruijssers A, Frierson J, Hooper L . Intestinal microbiota promote enteric virus replication and systemic pathogenesis. Science. 2011; 334(6053):249-52. PMC: 3222156. DOI: 10.1126/science.1211057. View

19.

Thackray L, Wobus C, Chachu K, Liu B, Alegre E, Henderson K . Murine noroviruses comprising a single genogroup exhibit biological diversity despite limited sequence divergence. J Virol. 2007; 81(19):10460-73. PMC: 2045448. DOI: 10.1128/JVI.00783-07. View

20.

Qin J, Li R, Raes J, Arumugam M, Burgdorf K, Manichanh C . A human gut microbial gene catalogue established by metagenomic sequencing. Nature. 2010; 464(7285):59-65. PMC: 3779803. DOI: 10.1038/nature08821. View