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The Interaction Between Viruses and Intestinal Microbiota: A Review

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Abstract

As the main pathogen threatening human and animal health, viruses can affect the immunity and metabolism of bodies. There are innate microbial barriers in the digestive tract of the body to preserve the homeostasis of the animal body, which directly or indirectly influences the host defence against viral infection. Understanding the interaction between viruses and intestinal microbiota or probiotics is helpful to study the pathogenesis of diseases. Here, we review recent studies on the interaction mechanism between intestinal microbiota and viruses. The interaction can be divided into two aspects: inhibition of viral infection by microbiota and promotion of viral infection by microbiota. The treatment of viral infection by probiotics is summarized.

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References

  1. Sekirov I, Russell SL, Antunes LC, Finlay BB (2010) Gut microbiota in health and disease. Physiol Rev 90(3):859–904. https://doi.org/10.1152/physrev.00045.2009

    Article  CAS  PubMed  Google Scholar 

  2. Frank DN, St Amand AL, Feldman RA, Boedeker EC, Harpaz N, Pace NR (2007) Molecular-phylogenetic characterization of microbial community imbalances in human inflammatory bowel diseases. Proc Natl Acad Sci U S A 104(34):13780–13785. https://doi.org/10.1073/pnas.0706625104

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Clemente JC, Ursell LK, Parfrey LW, Knight R (2012) The impact of the gut microbiota on human health: an integrative view. Cell 148(6):1258–1270. https://doi.org/10.1016/j.cell.2012.01.035

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Pitlik SD, Koren O (2017) How holobionts get sick-toward a unifying scheme of disease. Microbiome 5(1):64. https://doi.org/10.1186/s40168-017-0281-7

    Article  PubMed  PubMed Central  Google Scholar 

  5. Carroll D, Daszak P, Wolfe ND, Gao GF, Morel CM, Morzaria S, Pablos-Mendez A, Tomori O, Mazet JAK (2018) The global virome project. Science 359(6378):872–874. https://doi.org/10.1126/science.aap7463

    Article  CAS  PubMed  Google Scholar 

  6. Sun X, Winglee K, Gharaibeh RZ, Gauthier J, He Z, Tripathi P, Avram D, Bruner S, Fodor A, Jobin C (2018) Microbiota-derived metabolic factors reduce campylobacteriosis in mice. Gastroenterology 154(6):1751-1763 e1752. https://doi.org/10.1053/j.gastro.2018.01.042

    Article  CAS  PubMed  Google Scholar 

  7. Zhang Z, Tang H, Chen P, Xie H, Tao Y (2019) Demystifying the manipulation of host immunity, metabolism, and extraintestinal tumors by the gut microbiome. Signal Transduct Target Ther 4:41. https://doi.org/10.1038/s41392-019-0074-5

    Article  PubMed  PubMed Central  Google Scholar 

  8. Biswas A, Petnicki-Ocwieja T, Kobayashi KS (2012) Nod2: a key regulator linking microbiota to intestinal mucosal immunity. J Mol Med (Berl) 90(1):15–24. https://doi.org/10.1007/s00109-011-0802-y

    Article  CAS  Google Scholar 

  9. Tsay TB, Yang MC, Chen PH, Hsu CM, Chen LW (2011) Gut flora enhance bacterial clearance in lung through toll-like receptors 4. J Biomed Sci 18:68. https://doi.org/10.1186/1423-0127-18-68

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Xu D, Huang Y, Wang J (2015) Gut microbiota modulate the immune effect against hepatitis B virus infection. Eur J Clin Microbiol Infect Dis 34(11):2139–2147. https://doi.org/10.1007/s10096-015-2464-0

    Article  CAS  PubMed  Google Scholar 

  11. Tsai F, Coyle WJ (2009) The microbiome and obesity: is obesity linked to our gut flora? Curr Gastroenterol Rep 11(4):307–313. https://doi.org/10.1007/s11894-009-0045-z

    Article  PubMed  Google Scholar 

  12. Gerritsen J, Smidt H, Rijkers GT, de Vos WM (2011) Intestinal microbiota in human health and disease: the impact of probiotics. Genes Nutr 6(3):209–240. https://doi.org/10.1007/s12263-011-0229-7

    Article  PubMed  PubMed Central  Google Scholar 

  13. Dessi A, Pintus R, Marras S, Cesare Marincola F, De Magistris A, Fanos V (2016) Metabolomics in necrotizing enterocolitis: the state of the art. Expert Rev Mol Diagn 16(10):1053–1058. https://doi.org/10.1080/14737159.2016.1211933

    Article  CAS  PubMed  Google Scholar 

  14. Zhu W, Gregory JC, Org E, Buffa JA, Gupta N, Wang Z, Li L, Fu X, Wu Y, Mehrabian M, Sartor RB, McIntyre TM, Silverstein RL, Tang WHW, DiDonato JA, Brown JM, Lusis AJ, Hazen SL (2016) Gut microbial metabolite TMAO enhances platelet hyperreactivity and thrombosis risk. Cell 165(1):111–124. https://doi.org/10.1016/j.cell.2016.02.011

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Wang Z, Roberts AB, Buffa JA, Levison BS, Zhu W, Org E, Gu X, Huang Y, Zamanian-Daryoush M, Culley MK, DiDonato AJ, Fu X, Hazen JE, Krajcik D, DiDonato JA, Lusis AJ, Hazen SL (2015) Non-lethal inhibition of gut microbial trimethylamine production for the treatment of atherosclerosis. Cell 163(7):1585–1595. https://doi.org/10.1016/j.cell.2015.11.055

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Bian X, Tu P, Chi L, Gao B, Ru H, Lu K (2017) Saccharin induced liver inflammation in mice by altering the gut microbiota and its metabolic functions. Food Chem Toxicol 107(Pt B):530–539. https://doi.org/10.1016/j.fct.2017.04.045

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Bjorksten B (2004) Effects of intestinal microflora and the environment on the development of asthma and allergy. Springer Semin Immunopathol 25(3–4):257–270. https://doi.org/10.1007/s00281-003-0142-2

    Article  PubMed  Google Scholar 

  18. Wen W, Qi Z, Wang J (2020) The function and mechanism of enterovirus 71 (EV71) 3C protease. Curr Microbiol 77(9):1968–1975. https://doi.org/10.1007/s00284-020-02082-4

    Article  CAS  PubMed  Google Scholar 

  19. Vazquez-Castellanos JF, Serrano-Villar S, Jimenez-Hernandez N, Soto Del Rio MD, Gayo S, Rojo D, Ferrer M, Barbas C, Moreno S, Estrada V, Rattei T, Latorre A, Moya A, Gosalbes MJ (2018) Interplay between gut microbiota metabolism and inflammation in HIV infection. ISME J 12(8):1964–1976. https://doi.org/10.1038/s41396-018-0151-8

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Wang J, Li F, Wei H, Lian ZX, Sun R, Tian Z (2014) Respiratory influenza virus infection induces intestinal immune injury via microbiota-mediated Th17 cell-dependent inflammation. J Exp Med 211(12):2397–2410. https://doi.org/10.1084/jem.20140625

    Article  PubMed  PubMed Central  Google Scholar 

  21. Wu HJ, Ivanov II, Darce J, Hattori K, Shima T, Umesaki Y, Littman DR, Benoist C, Mathis D (2010) Gut-residing segmented filamentous bacteria drive autoimmune arthritis via T helper 17 cells. Immunity 32(6):815–827. https://doi.org/10.1016/j.immuni.2010.06.001

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Laude H, Rasschaert D, Delmas B, Godet M, Gelfi J, Charley B (1990) Molecular biology of transmissible gastroenteritis virus. Vet Microbiol 23(1–4):147–154. https://doi.org/10.1016/0378-1135(90)90144-k

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Xia L, Yang Y, Wang J, Jing Y, Yang Q (2018) Impact of TGEV infection on the pig small intestine. Virol J 15(1):102. https://doi.org/10.1186/s12985-018-1012-9

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Jang JY, Kim S, Kwon MS, Lee J, Yu DH, Song RH, Choi HJ, Park J (2019) Rotavirus-mediated alteration of gut microbiota and its correlation with physiological characteristics in neonatal calves. J Microbiol 57(2):113–121. https://doi.org/10.1007/s12275-019-8549-1

    Article  CAS  PubMed  Google Scholar 

  25. Li H, Liu X, Chen F, Zuo K, Wu C, Yan Y, Chen W, Lin W, Xie Q (2018) Avian influenza virus subtype H9N2 affects intestinal microbiota, barrier structure injury, and inflammatory intestinal disease in the chicken ileum. Viruses. https://doi.org/10.3390/v10050270

    Article  PubMed  PubMed Central  Google Scholar 

  26. Chen SY, Tsai CN, Lee YS, Lin CY, Huang KY, Chao HC, Lai MW, Chiu CH (2017) Intestinal microbiome in children with severe and complicated acute viral gastroenteritis. Sci Rep 7:46130. https://doi.org/10.1038/srep46130

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Sandhu KV, Sherwin E, Schellekens H, Stanton C, Dinan TG, Cryan JF (2017) Feeding the microbiota-gut-brain axis: diet, microbiome, and neuropsychiatry. Transl Res 179:223–244. https://doi.org/10.1016/j.trsl.2016.10.002

    Article  CAS  PubMed  Google Scholar 

  28. Borrelli L, Aceto S, Agnisola C, De Paolo S, Dipineto L, Stilling RM, Dinan TG, Cryan JF, Menna LF, Fioretti A (2016) Probiotic modulation of the microbiota-gut-brain axis and behaviour in zebrafish. Sci Rep 6:30046. https://doi.org/10.1038/srep30046

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Carrillo-Salinas FJ, Mestre L, Mecha M, Feliu A, Del Campo R, Villarrubia N, Espejo C, Montalban X, Alvarez-Cermeno JC, Villar LM, Guaza C (2017) Gut dysbiosis and neuroimmune responses to brain infection with Theiler’s murine encephalomyelitis virus. Sci Rep 7:44377. https://doi.org/10.1038/srep44377

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Shi Z, Zou J, Zhang Z, Zhao X, Noriega J, Zhang B, Zhao C, Ingle H, Bittinger K, Mattei LM, Pruijssers AJ, Plemper RK, Nice TJ, Baldridge MT, Dermody TS, Chassaing B, Gewirtz AT (2019) Segmented filamentous bacteria prevent and cure rotavirus infection. Cell 179(3):644-658 e613. https://doi.org/10.1016/j.cell.2019.09.028

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Antunes KH, Fachi JL, de Paula R, da Silva EF, Pral LP, Dos Santos AA, Dias GBM, Vargas JE, Puga R, Mayer FQ, Maito F, Zarate-Blades CR, Ajami NJ, Sant’Ana MR, Candreva T, Rodrigues HG, Schmiele M, Silva Clerici MTP, Proenca-Modena JL, Vieira AT, Mackay CR, Mansur D, Caballero MT, Marzec J, Li J, Wang X, Bell D, Polack FP, Kleeberger SR, Stein RT, Vinolo MAR, de Souza APD (2019) Microbiota-derived acetate protects against respiratory syncytial virus infection through a GPR43-type 1 interferon response. Nat Commun 10(1):3273. https://doi.org/10.1038/s41467-019-11152-6

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Lee H, Ko G (2016) Antiviral effect of vitamin A on norovirus infection via modulation of the gut microbiome. Sci Rep 6:25835. https://doi.org/10.1038/srep25835

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Thackray LB, Handley SA, Gorman MJ, Poddar S, Bagadia P, Briseno CG, Theisen DJ, Tan Q, Hykes BL Jr, Lin H, Lucas TM, Desai C, Gordon JI, Murphy KM, Virgin HW, Diamond MS (2018) Oral antibiotic treatment of mice exacerbates the disease severity of multiple flavivirus infections. Cell Rep 22(13):3440-3453 e3446. https://doi.org/10.1016/j.celrep.2018.03.001

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. York A (2018) Delivery of the gut microbiome. Nat Rev Microbiol 16(9):520–521. https://doi.org/10.1038/s41579-018-0059-3

    Article  CAS  PubMed  Google Scholar 

  35. Gonzalez-Perez G, Hicks AL, Tekieli TM, Radens CM, Williams BL, Lamouse-Smith ES (2016) Maternal antibiotic treatment impacts development of the neonatal intestinal microbiome and antiviral immunity. J Immunol 196(9):3768–3779. https://doi.org/10.4049/jimmunol.1502322

    Article  CAS  PubMed  Google Scholar 

  36. Zheng W, Zhao W, Wu M, Song X, Caro F, Sun X, Gazzaniga F, Stefanetti G, Oh S, Mekalanos JJ, Kasper DL (2020) Microbiota-targeted maternal antibodies protect neonates from enteric infection. Nature 577(7791):543–548. https://doi.org/10.1038/s41586-019-1898-4

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Qin N, Zheng B, Yao J, Guo L, Zuo J, Wu L, Zhou J, Liu L, Guo J, Ni S, Li A, Zhu Y, Liang W, Xiao Y, Ehrlich SD, Li L (2015) Influence of H7N9 virus infection and associated treatment on human gut microbiota. Sci Rep 5:14771. https://doi.org/10.1038/srep14771

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Uchiyama R, Chassaing B, Zhang B, Gewirtz AT (2014) Antibiotic treatment suppresses rotavirus infection and enhances specific humoral immunity. J Infect Dis 210(2):171–182. https://doi.org/10.1093/infdis/jiu037

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Jones MK, Watanabe M, Zhu S, Graves CL, Keyes LR, Grau KR, Gonzalez-Hernandez MB, Iovine NM, Wobus CE, Vinje J, Tibbetts SA, Wallet SM, Karst SM (2014) Enteric bacteria promote human and mouse norovirus infection of B cells. Science 346(6210):755–759. https://doi.org/10.1126/science.1257147

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Wilen CB, Lee S, Hsieh LL, Orchard RC, Desai C, Hykes BL Jr, McAllaster MR, Balce DR, Feehley T, Brestoff JR, Hickey CA, Yokoyama CC, Wang YT, MacDuff DA, Kreamalmayer D, Howitt MR, Neil JA, Cadwell K, Allen PM, Handley SA, van Lookeren CM, Baldridge MT, Virgin HW (2018) Tropism for tuft cells determines immune promotion of norovirus pathogenesis. Science 360(6385):204–208. https://doi.org/10.1126/science.aar3799

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Murakami K, Tenge VR, Karandikar UC, Lin SC, Ramani S, Ettayebi K, Crawford SE, Zeng XL, Neill FH, Ayyar BV, Katayama K, Graham DY, Bieberich E, Atmar RL, Estes MK (2020) Bile acids and ceramide overcome the entry restriction for GII.3 human norovirus replication in human intestinal enteroids. Proc Natl Acad Sci U S A 117(3):1700–1710. https://doi.org/10.1073/pnas.1910138117

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Kuss SK, Best GT, Etheredge CA, Pruijssers AJ, Frierson JM, Hooper LV, Dermody TS, Pfeiffer JK (2011) Intestinal microbiota promote enteric virus replication and systemic pathogenesis. Science 334(6053):249–252. https://doi.org/10.1126/science.1211057

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Erickson AK, Jesudhasan PR, Mayer MJ, Narbad A, Winter SE, Pfeiffer JK (2018) Bacteria facilitate enteric virus co-infection of mammalian cells and promote genetic recombination. Cell Host & Microbe 23(1):77–8875. https://doi.org/10.1016/j.chom.2017.11.007

    Article  CAS  Google Scholar 

  44. Robinson CM, Jesudhasan PR, Pfeiffer JK (2014) Bacterial lipopolysaccharide binding enhances virion stability and promotes environmental fitness of an enteric virus. Cell Host & Microbe 15(1):36–46. https://doi.org/10.1016/j.chom.2013.12.004

    Article  CAS  Google Scholar 

  45. Berger AK, Yi H, Kearns DB, Mainou BA (2017) Bacteria and bacterial envelope components enhance mammalian reovirus thermostability. PLoS Pathog 13(12):e1006768. https://doi.org/10.1371/journal.ppat.1006768

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Wu P, Sun P, Nie K, Zhu Y, Shi M, Xiao C, Liu H, Liu Q, Zhao T, Chen X, Zhou H, Wang P, Cheng G (2019) A gut commensal bacterium promotes mosquito permissiveness to arboviruses. Cell Host & Microbe 25(1):101–11105. https://doi.org/10.1016/j.chom.2018.11.004

    Article  CAS  Google Scholar 

  47. Pearson JA, Tai N, Ekanayake-Alper DK, Peng J, Hu Y, Hager K, Compton S, Wong FS, Smith PC, Wen L (2019) Norovirus changes susceptibility to type 1 diabetes by altering intestinal microbiota and immune cell functions. Front Immunol 10:2654. https://doi.org/10.3389/fimmu.2019.02654

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Grau KR, Zhu S, Peterson ST, Helm EW, Philip D, Phillips M, Hernandez A, Turula H, Frasse P, Graziano VR, Wilen CB, Wobus CE, Baldridge MT, Karst SM (2020) The intestinal regionalization of acute norovirus infection is regulated by the microbiota via bile acid-mediated priming of type III interferon. Nat Microbiol 5(1):84–92. https://doi.org/10.1038/s41564-019-0602-7

    Article  CAS  PubMed  Google Scholar 

  49. Engevik MA, Banks LD, Engevik KA, Chang-Graham AL, Perry JL, Hutchinson DS, Ajami NJ, Petrosino JF, Hyser JM (2020) Rotavirus infection induces glycan availability to promote ileum-specific changes in the microbiome aiding rotavirus virulence. Gut Microbes 11(5):1324–1347. https://doi.org/10.1080/19490976.2020.1754714

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Xia L, Dai L, Yu Q, Yang Q (2017) Persistent transmissible gastroenteritis virus infection enhances enterotoxigenic Escherichia coli K88 adhesion by promoting epithelial-mesenchymal transition in intestinal epithelial cells. J Virol. https://doi.org/10.1128/JVI.01256-17

    Article  PubMed  PubMed Central  Google Scholar 

  51. Lu J, Ma SS, Zhang WY, Duan JP (2019) Changes in peripheral blood inflammatory factors (TNF-alpha and IL-6) and intestinal flora in AIDS and HIV-positive individuals. J Zhejiang Univ Sci B 20(10):793–802. https://doi.org/10.1631/jzus.B1900075

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Dillon SM, Lee EJ, Donovan AM, Guo K, Harper MS, Frank DN, McCarter MD, Santiago ML, Wilson CC (2016) Enhancement of HIV-1 infection and intestinal CD4+ T cell depletion ex vivo by gut microbes altered during chronic HIV-1 infection. Retrovirology 13:5. https://doi.org/10.1186/s12977-016-0237-1

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Tuddenham SA, Koay WLA, Zhao N, White JR, Ghanem KG, Sears CL, Consortium HIVMR-a (2020) The impact of human immunodeficiency virus infection on gut microbiota alpha-diversity: an individual-level meta-analysis. Clin Infect Dis 70(4):615–627. https://doi.org/10.1093/cid/ciz258

    Article  PubMed  Google Scholar 

  54. Mudd JC, Brenchley JM (2016) Gut mucosal barrier dysfunction, microbial dysbiosis, and their role in HIV-1 disease progression. J Infect Dis 214(Suppl 2):S58-66. https://doi.org/10.1093/infdis/jiw258

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Harding JN, Siefker D, Vu L, You D, DeVincenzo J, Pierre JF, Cormier SA (2020) Altered gut microbiota in infants is associated with respiratory syncytial virus disease severity. BMC Microbiol 20(1):140. https://doi.org/10.1186/s12866-020-01816-5

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Abdelhamid AG, El-Masry SS, El-Dougdoug NK (2019) Probiotic lactobacillus and bifidobacterium strains possess safety characteristics, antiviral activities and host adherence factors revealed by genome mining. EPMA J 10(4):337–350. https://doi.org/10.1007/s13167-019-00184-z

    Article  PubMed  PubMed Central  Google Scholar 

  57. Wang X, Hu W, Zhu L, Yang Q (2017) Bacillus subtilis and surfactin inhibit the transmissible gastroenteritis virus from entering the intestinal epithelial cells. Biosci Rep. https://doi.org/10.1042/BSR20170082

  58. Kanmani P, Albarracin L, Kobayashi H, Iida H, Komatsu R, Humayun Kober AKM, Ikeda-Ohtsubo W, Suda Y, Aso H, Makino S, Kano H, Saito T, Villena J, Kitazawa H (2018) Exopolysaccharides from lactobacillus delbrueckii OLL1073R-1 modulate innate antiviral immune response in porcine intestinal epithelial cells. Mol Immunol 93:253–265. https://doi.org/10.1016/j.molimm.2017.07.009

    Article  CAS  PubMed  Google Scholar 

  59. Nealon NJ, Yuan L, Yang X, Ryan EP (2017) Rice bran and probiotics alter the porcine large intestine and serum metabolomes for protection against human rotavirus diarrhea. Front Microbiol 8:653. https://doi.org/10.3389/fmicb.2017.00653

    Article  PubMed  PubMed Central  Google Scholar 

  60. Park MS, Kwon B, Ku S, Ji GE (2017) The efficacy of Bifidobacterium longum BORI and Lactobacillus acidophilus AD031 probiotic treatment in infants with rotavirus infection. Nutrients. https://doi.org/10.3390/nu9080887

    Article  PubMed  PubMed Central  Google Scholar 

  61. Chai W, Burwinkel M, Wang Z, Palissa C, Esch B, Twardziok S, Rieger J, Wrede P, Schmidt MF (2013) Antiviral effects of a probiotic Enterococcus faecium strain against transmissible gastroenteritis coronavirus. Arch Virol 158(4):799–807. https://doi.org/10.1007/s00705-012-1543-0

    Article  CAS  PubMed  Google Scholar 

  62. Kumar R, Seo BJ, Mun MR, Kim CJ, Lee I, Kim H, Park YH (2010) Putative probiotic Lactobacillus spp. from porcine gastrointestinal tract inhibit transmissible gastroenteritis coronavirus and enteric bacterial pathogens. Trop Anim Health Prod 42(8):1855–1860. https://doi.org/10.1007/s11250-010-9648-5

    Article  PubMed  Google Scholar 

  63. Alqazlan N, Alizadeh M, Boodhoo N, Taha-Abdelaziz K, Nagy E, Bridle B, Sharif S (2020) Probiotic lactobacilli limit avian influenza virus subtype H9N2 replication in chicken cecal tonsil mononuclear cells. Vaccines (Basel). https://doi.org/10.3390/vaccines8040605

    Article  Google Scholar 

  64. Ermolenko EI, Desheva YA, Kolobov AA, Kotyleva MP, Sychev IA, Suvorov AN (2019) Anti-influenza activity of enterocin B in vitro and protective effect of bacteriocinogenic enterococcal probiotic strain on influenza infection in mouse model. Probiotics Antimicrob Proteins 11(2):705–712. https://doi.org/10.1007/s12602-018-9457-0

    Article  CAS  PubMed  Google Scholar 

  65. Eguchi K, Fujitani N, Nakagawa H, Miyazaki T (2019) Prevention of respiratory syncytial virus infection with probiotic lactic acid bacterium Lactobacillus gasseri SBT2055. Sci Rep 9(1):4812. https://doi.org/10.1038/s41598-019-39602-7

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Waiyamitra P, Zoral MA, Saengtienchai A, Luengnaruemitchai A, Decamp O, Gorgoglione B, Surachetpong W (2020) Probiotics modulate tilapia resistance and immune response against tilapia lake virus infection. Pathogens. https://doi.org/10.3390/pathogens9110919

    Article  PubMed  PubMed Central  Google Scholar 

  67. Cantu-Bernal S, Dominguez-Gamez M, Medina-Peraza I, Aros-Uzarraga E, Ontiveros N, Flores-Mendoza L, Gomez-Flores R, Tamez-Guerra P, Gonzalez-Ochoa G (2020) Enhanced viability and anti-rotavirus effect of Bifidobacterium longum and Lactobacillus plantarum in combination with Chlorella sorokiniana in a dairy product. Front Microbiol 11:875. https://doi.org/10.3389/fmicb.2020.00875

    Article  PubMed  PubMed Central  Google Scholar 

  68. Barrangou R, Horvath P (2017) A decade of discovery: CRISPR functions and applications. Nat Microbiol 2:17092. https://doi.org/10.1038/nmicrobiol.2017.92

    Article  CAS  PubMed  Google Scholar 

  69. Starosila D, Rybalko S, Varbanetz L, Ivanskaya N, Sorokulova I (2017) Anti-influenza activity of a Bacillus subtilis probiotic strain. Antimicrob Agents Chemother. https://doi.org/10.1128/AAC.00539-17

    Article  PubMed  PubMed Central  Google Scholar 

  70. Ingle H, Lee S, Ai T, Orvedahl A, Rodgers R, Zhao G, Sullender M, Peterson ST, Locke M, Liu TC, Yokoyama CC, Sharp B, Schultz-Cherry S, Miner JJ, Baldridge MT (2019) Viral complementation of immunodeficiency confers protection against enteric pathogens via interferon-lambda. Nat Microbiol 4(7):1120–1128. https://doi.org/10.1038/s41564-019-0416-7

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Pereira GQ, Gomes LA, Santos IS, Alfieri AF, Weese JS, Costa MC (2018) Fecal microbiota transplantation in puppies with canine parvovirus infection. J Vet Intern Med 32(2):707–711. https://doi.org/10.1111/jvim.15072

    Article  PubMed  PubMed Central  Google Scholar 

  72. Nakayama Y, Moriya T, Sakai F, Ikeda N, Shiozaki T, Hosoya T, Nakagawa H, Miyazaki T (2014) Oral administration of Lactobacillus gasseri SBT2055 is effective for preventing influenza in mice. Sci Rep 4:4638. https://doi.org/10.1038/srep04638

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Inatomi T, Amatatsu M, Romero-Perez GA, Inoue R, Tsukahara T (2017) Dietary probiotic compound improves reproductive performance of porcine epidemic diarrhea virus-infected sows reared in a Japanese commercial swine farm under vaccine control condition. Front Immunol 8:1877. https://doi.org/10.3389/fimmu.2017.01877

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Reimer RA (2019) Establishing the role of diet in the microbiota-disease axis. Nat Rev Gastroenterol Hepatol 16(2):86–87. https://doi.org/10.1038/s41575-018-0093-7

    Article  PubMed  Google Scholar 

  75. Leonard SP, Powell JE, Perutka J, Geng P, Heckmann LC, Horak RD, Davies BW, Ellington AD, Barrick JE, Moran NA (2020) Engineered symbionts activate honey bee immunity and limit pathogens. Science 367(6477):573–576. https://doi.org/10.1126/science.aax9039

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. Oo KM, Lwin AA, Kyaw YY, Tun WM, Fukada K, Goshima A, Shimada T, Okada S (2016) Safety and long-term effect of the probiotic FK-23 in patients with hepatitis C virus infection. Biosci Microbiota Food Health 35(3):123–128. https://doi.org/10.12938/bmfh.2015-024

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Cunningham-Rundles S, Ahrne S, Bengmark S, Johann-Liang R, Marshall F, Metakis L, Califano C, Dunn AM, Grassey C, Hinds G, Cervia J (2000) Probiotics and immune response. Am J Gastroenterol 95(1 Suppl):S22-25. https://doi.org/10.1016/s0002-9270(99)00813-8

    Article  CAS  PubMed  Google Scholar 

  78. Gleeson M, Bishop NC, Struszczak L (2016) Effects of Lactobacillus casei Shirota ingestion on common cold infection and herpes virus antibodies in endurance athletes: a placebo-controlled, randomized trial. Eur J Appl Physiol 116(8):1555–1563. https://doi.org/10.1007/s00421-016-3415-x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Ishizaki A, Bi X, Nguyen LV, Matsuda K, Pham HV, Phan CTT, Khu DTK, Ichimura H (2017) Effects of short-term probiotic ingestion on immune profiles and microbial translocation among HIV-1-infected Vietnamese children. Int J Mol Sci. https://doi.org/10.3390/ijms18102185

    Article  PubMed  PubMed Central  Google Scholar 

  80. Nagata S, Asahara T, Ohta T, Yamada T, Kondo S, Bian L, Wang C, Yamashiro Y, Nomoto K (2011) Effect of the continuous intake of probiotic-fermented milk containing Lactobacillus casei strain Shirota on fever in a mass outbreak of norovirus gastroenteritis and the faecal microflora in a health service facility for the aged. Br J Nutr 106(4):549–556. https://doi.org/10.1017/S000711451100064X

    Article  CAS  PubMed  Google Scholar 

  81. Luoto R, Ruuskanen O, Waris M, Kalliomaki M, Salminen S, Isolauri E (2014) Prebiotic and probiotic supplementation prevents rhinovirus infections in preterm infants: a randomized, placebo-controlled trial. J Allergy Clin Immunol 133(2):405–413. https://doi.org/10.1016/j.jaci.2013.08.020

    Article  PubMed  Google Scholar 

  82. Sindhu KN, Sowmyanarayanan TV, Paul A, Babji S, Ajjampur SS, Priyadarshini S, Sarkar R, Balasubramanian KA, Wanke CA, Ward HD, Kang G (2014) Immune response and intestinal permeability in children with acute gastroenteritis treated with Lactobacillus rhamnosus GG: a randomized, double-blind, placebo-controlled trial. Clin Infect Dis 58(8):1107–1115. https://doi.org/10.1093/cid/ciu065

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. Lappin MR, Veir JK, Satyaraj E, Czarnecki-Maulden G (2009) Pilot study to evaluate the effect of oral supplementation of Enterococcus faecium SF68 on cats with latent feline herpesvirus 1. J Feline Med Surg 11(8):650–654. https://doi.org/10.1016/j.jfms.2008.12.006

    Article  PubMed  Google Scholar 

  84. Sarker SA, Sultana S, Fuchs GJ, Alam NH, Azim T, Brussow H, Hammarstrom L (2005) Lactobacillus paracasei strain ST11 has no effect on rotavirus but ameliorates the outcome of nonrotavirus diarrhea in children from Bangladesh. Pediatrics 116(2):e221-228. https://doi.org/10.1542/peds.2004-2334

    Article  PubMed  Google Scholar 

  85. Shinkai S, Toba M, Saito T, Sato I, Tsubouchi M, Taira K, Kakumoto K, Inamatsu T, Yoshida H, Fujiwara Y, Fukaya T, Matsumoto T, Tateda K, Yamaguchi K, Kohda N, Kohno S (2013) Immunoprotective effects of oral intake of heat-killed Lactobacillus pentosus strain b240 in elderly adults: a randomised, double-blind, placebo-controlled trial. Br J Nutr 109(10):1856–1865. https://doi.org/10.1017/S0007114512003753

    Article  CAS  PubMed  Google Scholar 

  86. Xia X, Chen J, Xia J, Wang B, Liu H, Yang L, Wang Y, Ling Z (2018) Role of probiotics in the treatment of minimal hepatic encephalopathy in patients with HBV-induced liver cirrhosis. J Int Med Res 46(9):3596–3604. https://doi.org/10.1177/0300060518776064

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  87. Holscher HD, Czerkies LA, Cekola P, Litov R, Benbow M, Santema S, Alexander DD, Perez V, Sun S, Saavedra JM, Tappenden KA (2012) Bifidobacterium lactis Bb12 enhances intestinal antibody response in formula-fed infants: a randomized, double-blind, controlled trial. J Parenter Enteral Nutr 36(1 Suppl):106S-117S. https://doi.org/10.1177/0148607111430817

    Article  CAS  Google Scholar 

  88. Narayanappa D (2008) Randomized double blinded controlled trial to evaluate the efficacy and safety of bifilac in patients with acute viral diarrhea. Indian J Pediatr 75(7):709–713. https://doi.org/10.1007/s12098-008-0134-2

    Article  CAS  PubMed  Google Scholar 

  89. Das S, Gupta PK, Das RR (2016) Efficacy and safety of Saccharomyces boulardii in acute rotavirus diarrhea: double blind randomized controlled trial from a developing country. J Trop Pediatr 62(6):464–470. https://doi.org/10.1093/tropej/fmw032

    Article  PubMed  Google Scholar 

  90. Magwira CA, Taylor MB (2018) Composition of gut microbiota and its influence on the immunogenicity of oral rotavirus vaccines. Vaccine 36(24):3427–3433. https://doi.org/10.1016/j.vaccine.2018.04.091

    Article  CAS  PubMed  Google Scholar 

  91. Harris VC, Armah G, Fuentes S, Korpela KE, Parashar U, Victor JC, Tate J, de Weerth C, Giaquinto C, Wiersinga WJ, Lewis KD, de Vos WM (2017) Significant correlation between the infant gut microbiome and rotavirus vaccine response in Rural Ghana. J Infect Dis 215(1):34–41. https://doi.org/10.1093/infdis/jiw518 (Epub 2016 Oct 31)

    Article  CAS  PubMed  Google Scholar 

  92. Michael H, Langel SN, Miyazaki A, Paim FC, Chepngeno J, Alhamo MA, Fischer DD, Srivastava V, Kathayat D, Deblais L, Rajashekara G, Saif LJ, Vlasova AN (2020) Malnutrition decreases antibody secreting cell numbers induced by an oral attenuated human rotavirus vaccine in a human infant fecal microbiota transplanted gnotobiotic pig model. Front Immunol 11:196. https://doi.org/10.3389/fimmu.2020.00196

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  93. Twitchell EL, Tin C, Wen K, Zhang H, Becker-Dreps S, Azcarate-Peril MA, Vilchez S, Li G, Ramesh A, Weiss M, Lei S, Bui T, Yang X, Schultz-Cherry S, Yuan L (2016) Modeling human enteric dysbiosis and rotavirus immunity in gnotobiotic pigs. Gut Pathog 8:51. https://doi.org/10.1186/s13099-016-0136-y

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  94. Harris V, Ali A, Fuentes S, Korpela K, Kazi M, Tate J, Parashar U, Wiersinga WJ, Giaquinto C, de Weerth C, de Vos WM (2018) Rotavirus vaccine response correlates with the infant gut microbiota composition in Pakistan. Gut Microbes 9(2):93–101. https://doi.org/10.1080/19490976.2017.1376162

    Article  CAS  PubMed  Google Scholar 

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Funding

This work was financially supported by the National Natural Science Foundation of China (Grant Nos. 31772809; 31872538); This work was also supported by National Key Research and Development Program Projects of China (2017YFD0500305, 2017YFD0500901), the National Key Program for Infectious Disease of China (2018ZX10101002-002), the State Key Program of National Natural Science of China (U1808202), NSFC International (Regional) Cooperation and Exchange program (31961143024), and Major science and technology projects of Inner Mongolia of China.

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  1. Key Laboratory of Zoonosis of Liaoning Province, College of Animal Science & Veterinary Medicine, Shenyang Agricultural University, Shenyang, 110866, China

    Zhiming Lv, Dongwei Xiong, Miao Long & Zeliang Chen

  2. Liaoning Service Development Center, Shenyang, China

    Jichao Shi

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  1. Zhiming Lv
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  2. Dongwei Xiong
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  3. Jichao Shi
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  4. Miao Long
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  5. Zeliang Chen
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Z.L wrote the paper; D.X. and J. S. revised the paper; M.L. and Z.C reviewed and edited the paper.

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Correspondence to Miao Long or Zeliang Chen.

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Lv, Z., Xiong, D., Shi, J. et al. The Interaction Between Viruses and Intestinal Microbiota: A Review. Curr Microbiol 78, 3597–3608 (2021). https://doi.org/10.1007/s00284-021-02623-5

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  • DOI: https://doi.org/10.1007/s00284-021-02623-5