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Published in: Virology Journal 1/2019

Open Access 01-12-2019 | Antibiotic | Research

The altered gut virome community in rhesus monkeys is correlated with the gut bacterial microbiome and associated metabolites

Authors: Heng Li, Hongzhe Li, Jingjing Wang, Lei Guo, Haitao Fan, Huiwen Zheng, Zening Yang, Xing Huang, Manman Chu, Fengmei Yang, Zhanlong He, Nan Li, Jinxi Yang, Qiongwen Wu, Haijing Shi, Longding Liu

Published in: Virology Journal | Issue 1/2019

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Abstract

Background

The gut microbiome is closely associated with the health of the host; although the interaction between the bacterial microbiome and the whole virome has rarely been studied, it is likely of medical importance. Examination of the interactions between the gut bacterial microbiome and virome of rhesus monkey would significantly contribute to revealing the gut microbiome composition.

Methods

Here, we conducted a metagenomic analysis of the gut microbiome of rhesus monkeys in a longitudinal cohort treated with an antibiotic cocktail, and we documented the interactions between the bacterial microbiome and virome. The depletion of viral populations was confirmed at the species level by real-time PCR. We also detected changes in the gut metabolome by GC-MS and LC-MS.

Results

A majority of bacteria were depleted after treatment with antibiotics, and the Shannon diversity index decreased from 2.95 to 0.22. Furthermore, the abundance-based coverage estimator (ACE) decreased from 104.47 to 33.84, and the abundance of eukaryotic viruses also changed substantially. In the annotation, 6 families of DNA viruses and 1 bacteriophage family were present in the normal monkeys but absent after gut bacterial microbiome depletion. Intriguingly, we discovered that changes in the gut bacterial microbiome composition may promote changes in the gut virome composition, and tryptophan, arginine, and quinone may play roles in the interaction between the bacterial microbiome and virome.

Conclusion

Our results indicated that the clearly altered composition of the virome was correlated with depletion in the bacterial community and that metabolites produced by bacteria possibly play important roles in the interaction.
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Literature
1.
go back to reference Dahiya DK, Renuka, Puniya M, Shandilya UK, Dhewa T, Kumar N, Kumar S, Puniya AK, Shukla P: Gut Microbiota Modulation and Its Relationship with Obesity Using Prebiotic Fibers and Probiotics: A Review Front Microbiol 2017, 8:563. Dahiya DK, Renuka, Puniya M, Shandilya UK, Dhewa T, Kumar N, Kumar S, Puniya AK, Shukla P: Gut Microbiota Modulation and Its Relationship with Obesity Using Prebiotic Fibers and Probiotics: A Review Front Microbiol 2017, 8:563.
3.
go back to reference Konturek PC, Brzozowski T, Konturek SJ. Stress and the gut: pathophysiology, clinical consequences, diagnostic approach and treatment options. J Physiol Pharmacol. 2011;62(6):591–9.PubMed Konturek PC, Brzozowski T, Konturek SJ. Stress and the gut: pathophysiology, clinical consequences, diagnostic approach and treatment options. J Physiol Pharmacol. 2011;62(6):591–9.PubMed
5.
go back to reference Turnbaugh PJ, Ley RE, Mahowald MA, Magrini V, Mardis ER, Gordon JI. An obesity-associated gut microbiome with increased capacity for energy harvest. Nature. 2006;444(7122):1027–31.PubMedCrossRef Turnbaugh PJ, Ley RE, Mahowald MA, Magrini V, Mardis ER, Gordon JI. An obesity-associated gut microbiome with increased capacity for energy harvest. Nature. 2006;444(7122):1027–31.PubMedCrossRef
6.
go back to reference Hsiao EY, McBride SW, Hsien S, Sharon G, Hyde ER, McCue T, Codelli JA, Chow J, Reisman SE, Petrosino JF, et al. Microbiota modulate behavioral and physiological abnormalities associated with neurodevelopmental disorders. Cell. 2013;155(7):1451–63.PubMedPubMedCentralCrossRef Hsiao EY, McBride SW, Hsien S, Sharon G, Hyde ER, McCue T, Codelli JA, Chow J, Reisman SE, Petrosino JF, et al. Microbiota modulate behavioral and physiological abnormalities associated with neurodevelopmental disorders. Cell. 2013;155(7):1451–63.PubMedPubMedCentralCrossRef
7.
go back to reference van Nood E, Vrieze A, Nieuwdorp M, Fuentes S, Zoetendal EG, de Vos WM, Visser CE, Kuijper EJ, Bartelsman JF, Tijssen JG, et al. Duodenal infusion of donor feces for recurrent Clostridium difficile. N Engl J Med. 2013;368(5):407–15.PubMedCrossRef van Nood E, Vrieze A, Nieuwdorp M, Fuentes S, Zoetendal EG, de Vos WM, Visser CE, Kuijper EJ, Bartelsman JF, Tijssen JG, et al. Duodenal infusion of donor feces for recurrent Clostridium difficile. N Engl J Med. 2013;368(5):407–15.PubMedCrossRef
8.
go back to reference Kelly CR, Kahn S, Kashyap P, Laine L, Rubin D, Atreja A, Moore T, Wu G. Update on fecal microbiota transplantation 2015: indications, methodologies, mechanisms, and outlook. Gastroenterology. 2015;149(1):223–37.PubMedCrossRef Kelly CR, Kahn S, Kashyap P, Laine L, Rubin D, Atreja A, Moore T, Wu G. Update on fecal microbiota transplantation 2015: indications, methodologies, mechanisms, and outlook. Gastroenterology. 2015;149(1):223–37.PubMedCrossRef
9.
go back to reference Minot S, Sinha R, Chen J, Li H, Keilbaugh SA, Wu GD, Lewis JD, Bushman FD. The human gut virome: inter-individual variation and dynamic response to diet. Genome Res. 2011;21(10):1616–25.PubMedPubMedCentralCrossRef Minot S, Sinha R, Chen J, Li H, Keilbaugh SA, Wu GD, Lewis JD, Bushman FD. The human gut virome: inter-individual variation and dynamic response to diet. Genome Res. 2011;21(10):1616–25.PubMedPubMedCentralCrossRef
10.
go back to reference Reyes A, Semenkovich NP, Whiteson K, Rohwer F, Gordon JI. Going viral: next-generation sequencing applied to phage populations in the human gut. Nat Rev Microbiol. 2012;10(9):607–17.PubMedPubMedCentralCrossRef Reyes A, Semenkovich NP, Whiteson K, Rohwer F, Gordon JI. Going viral: next-generation sequencing applied to phage populations in the human gut. Nat Rev Microbiol. 2012;10(9):607–17.PubMedPubMedCentralCrossRef
11.
go back to reference Duerkop BA, Clements CV, Rollins D, Rodrigues JL, Hooper LV. A composite bacteriophage alters colonization by an intestinal commensal bacterium. Proc Natl Acad Sci U S A. 2012;109(43):17621–6.PubMedPubMedCentralCrossRef Duerkop BA, Clements CV, Rollins D, Rodrigues JL, Hooper LV. A composite bacteriophage alters colonization by an intestinal commensal bacterium. Proc Natl Acad Sci U S A. 2012;109(43):17621–6.PubMedPubMedCentralCrossRef
12.
go back to reference Barr JJ, Auro R, Furlan M, Whiteson KL, Erb ML, Pogliano J, Stotland A, Wolkowicz R, Cutting AS, Doran KS, et al. Bacteriophage adhering to mucus provide a non-host-derived immunity. Proc Natl Acad Sci U S A. 2013;110(26):10771–6.PubMedPubMedCentralCrossRef Barr JJ, Auro R, Furlan M, Whiteson KL, Erb ML, Pogliano J, Stotland A, Wolkowicz R, Cutting AS, Doran KS, et al. Bacteriophage adhering to mucus provide a non-host-derived immunity. Proc Natl Acad Sci U S A. 2013;110(26):10771–6.PubMedPubMedCentralCrossRef
13.
go back to reference Barton ES, White DW, Cathelyn JS, Brett-McClellan KA, Engle M, Diamond MS, Miller VL, Virgin HW. Herpesvirus latency confers symbiotic protection from bacterial infection. Nature. 2007;447(7142):326–9.PubMedCrossRef Barton ES, White DW, Cathelyn JS, Brett-McClellan KA, Engle M, Diamond MS, Miller VL, Virgin HW. Herpesvirus latency confers symbiotic protection from bacterial infection. Nature. 2007;447(7142):326–9.PubMedCrossRef
15.
go back to reference He Q, Gao Y, Jie Z, Yu X, Laursen JM, Xiao L, Li Y, Li L, Zhang F, Feng Q, et al. Two distinct metacommunities characterize the gut microbiota in Crohn's disease patients. Gigascience. 2017;6(7):1–11.PubMedPubMedCentralCrossRef He Q, Gao Y, Jie Z, Yu X, Laursen JM, Xiao L, Li Y, Li L, Zhang F, Feng Q, et al. Two distinct metacommunities characterize the gut microbiota in Crohn's disease patients. Gigascience. 2017;6(7):1–11.PubMedPubMedCentralCrossRef
16.
go back to reference Chehoud C, Dryga A, Hwang Y, Nagy-Szakal D, Hollister EB, Luna RA, Versalovic J, Kellermayer R, Bushman FD. Transfer of viral communities between human individuals during fecal microbiota transplantation. MBio. 2016;7(2):e00322.PubMedPubMedCentralCrossRef Chehoud C, Dryga A, Hwang Y, Nagy-Szakal D, Hollister EB, Luna RA, Versalovic J, Kellermayer R, Bushman FD. Transfer of viral communities between human individuals during fecal microbiota transplantation. MBio. 2016;7(2):e00322.PubMedPubMedCentralCrossRef
17.
go back to reference Reyes A, Haynes M, Hanson N, Angly FE, Heath AC, Rohwer F, Gordon JI. Viruses in the faecal microbiota of monozygotic twins and their mothers. Nature. 2010;466(7304):334–8.PubMedPubMedCentralCrossRef Reyes A, Haynes M, Hanson N, Angly FE, Heath AC, Rohwer F, Gordon JI. Viruses in the faecal microbiota of monozygotic twins and their mothers. Nature. 2010;466(7304):334–8.PubMedPubMedCentralCrossRef
18.
go back to reference Siegel SJ, Roche AM, Weiser JN. Influenza promotes pneumococcal growth during coinfection by providing host sialylated substrates as a nutrient source. Cell Host Microbe. 2014;16(1):55–67.PubMedPubMedCentralCrossRef Siegel SJ, Roche AM, Weiser JN. Influenza promotes pneumococcal growth during coinfection by providing host sialylated substrates as a nutrient source. Cell Host Microbe. 2014;16(1):55–67.PubMedPubMedCentralCrossRef
19.
go back to reference Khan MN, Xu Q, Pichichero ME. Protection against Streptococcus pneumoniae Invasive Pathogenesis by a Protein-Based Vaccine Is Achieved by Suppression of Nasiopharyngeal Bacterial Density during Influenza A Virus Coinfection. Infect Immun. 2017;85(2):e00530-16. Khan MN, Xu Q, Pichichero ME. Protection against Streptococcus pneumoniae Invasive Pathogenesis by a Protein-Based Vaccine Is Achieved by Suppression of Nasiopharyngeal Bacterial Density during Influenza A Virus Coinfection. Infect Immun. 2017;85(2):e00530-16.
20.
go back to reference Handley SA, Desai C, Zhao G, Droit L, Monaco CL, Schroeder AC, Nkolola JP, Norman ME, Miller AD, Wang D, et al. SIV infection-mediated changes in gastrointestinal bacterial microbiome and Virome are associated with immunodeficiency and prevented by vaccination. Cell Host Microbe. 2016;19(3):323–35.PubMedPubMedCentralCrossRef Handley SA, Desai C, Zhao G, Droit L, Monaco CL, Schroeder AC, Nkolola JP, Norman ME, Miller AD, Wang D, et al. SIV infection-mediated changes in gastrointestinal bacterial microbiome and Virome are associated with immunodeficiency and prevented by vaccination. Cell Host Microbe. 2016;19(3):323–35.PubMedPubMedCentralCrossRef
21.
go back to reference Deriu E, Boxx GM, He X, Pan C, Benavidez SD, Cen L, Rozengurt N, Shi W, Cheng G. Influenza virus affects intestinal microbiota and secondary Salmonella infection in the gut through type I interferons. PLoS Pathog. 2016;12(5):e1005572.PubMedPubMedCentralCrossRef Deriu E, Boxx GM, He X, Pan C, Benavidez SD, Cen L, Rozengurt N, Shi W, Cheng G. Influenza virus affects intestinal microbiota and secondary Salmonella infection in the gut through type I interferons. PLoS Pathog. 2016;12(5):e1005572.PubMedPubMedCentralCrossRef
22.
go back to reference Jones MK, Watanabe M, Zhu S, Graves CL, Keyes LR, Grau KR, Gonzalez-Hernandez MB, Iovine NM, Wobus CE, Vinje J, et al. Enteric bacteria promote human and mouse norovirus infection of B cells. Science. 2014;346(6210):755–9.PubMedPubMedCentralCrossRef Jones MK, Watanabe M, Zhu S, Graves CL, Keyes LR, Grau KR, Gonzalez-Hernandez MB, Iovine NM, Wobus CE, Vinje J, et al. Enteric bacteria promote human and mouse norovirus infection of B cells. Science. 2014;346(6210):755–9.PubMedPubMedCentralCrossRef
24.
go back to reference Ichinohe T, Pang IK, Kumamoto Y, Peaper DR, Ho JH, Murray TS, Iwasaki A. Microbiota regulates immune defense against respiratory tract influenza a virus infection. Proc Natl Acad Sci U S A. 2011;108(13):5354–9.PubMedPubMedCentralCrossRef Ichinohe T, Pang IK, Kumamoto Y, Peaper DR, Ho JH, Murray TS, Iwasaki A. Microbiota regulates immune defense against respiratory tract influenza a virus infection. Proc Natl Acad Sci U S A. 2011;108(13):5354–9.PubMedPubMedCentralCrossRef
25.
go back to reference Reyes A, Wu M, McNulty NP, Rohwer FL, Gordon JI. Gnotobiotic mouse model of phage-bacterial host dynamics in the human gut. Proc Natl Acad Sci U S A. 2013;110(50):20236–41.PubMedPubMedCentralCrossRef Reyes A, Wu M, McNulty NP, Rohwer FL, Gordon JI. Gnotobiotic mouse model of phage-bacterial host dynamics in the human gut. Proc Natl Acad Sci U S A. 2013;110(50):20236–41.PubMedPubMedCentralCrossRef
26.
go back to reference Lim ES, Zhou Y, Zhao G, Bauer IK, Droit L, Ndao IM, Warner BB, Tarr PI, Wang D, Holtz LR. Early life dynamics of the human gut virome and bacterial microbiome in infants. Nat Med. 2015;21(10):1228–34.PubMedPubMedCentralCrossRef Lim ES, Zhou Y, Zhao G, Bauer IK, Droit L, Ndao IM, Warner BB, Tarr PI, Wang D, Holtz LR. Early life dynamics of the human gut virome and bacterial microbiome in infants. Nat Med. 2015;21(10):1228–34.PubMedPubMedCentralCrossRef
27.
go back to reference Lv Z, Peng G, Liu W, Xu H, Su J. Berberine blocks the relapse of Clostridium difficile infection in C57BL/6 mice after standard vancomycin treatment. Antimicrob Agents Chemother. 2015;59(7):3726–35.PubMedPubMedCentralCrossRef Lv Z, Peng G, Liu W, Xu H, Su J. Berberine blocks the relapse of Clostridium difficile infection in C57BL/6 mice after standard vancomycin treatment. Antimicrob Agents Chemother. 2015;59(7):3726–35.PubMedPubMedCentralCrossRef
28.
go back to reference Hsiao A, Ahmed AM, Subramanian S, Griffin NW, Drewry LL, Petri WA Jr, Haque R, Ahmed T, Gordon JI. Members of the human gut microbiota involved in recovery from Vibrio cholerae infection. Nature. 2014;515(7527):423–6.PubMedPubMedCentralCrossRef Hsiao A, Ahmed AM, Subramanian S, Griffin NW, Drewry LL, Petri WA Jr, Haque R, Ahmed T, Gordon JI. Members of the human gut microbiota involved in recovery from Vibrio cholerae infection. Nature. 2014;515(7527):423–6.PubMedPubMedCentralCrossRef
29.
go back to reference Langille MG, Zaneveld J, Caporaso JG, McDonald D, Knights D, Reyes JA, Clemente JC, Burkepile DE, Vega Thurber RL, Knight R, et al. Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nat Biotechnol. 2013;31(9):814–21.PubMedPubMedCentralCrossRef Langille MG, Zaneveld J, Caporaso JG, McDonald D, Knights D, Reyes JA, Clemente JC, Burkepile DE, Vega Thurber RL, Knight R, et al. Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nat Biotechnol. 2013;31(9):814–21.PubMedPubMedCentralCrossRef
30.
go back to reference Arboleya S, Sanchez B, Solis G, Fernandez N, Suarez M, Hernandez-Barranco AM, Milani C, Margolles A, de Los Reyes-Gavilan CG, Ventura M et al: Impact of Prematurity and Perinatal Antibiotics on the Developing Intestinal Microbiota: A Functional Inference Study. Int J Mol Sci 2016, 17(5).PubMedCentralCrossRef Arboleya S, Sanchez B, Solis G, Fernandez N, Suarez M, Hernandez-Barranco AM, Milani C, Margolles A, de Los Reyes-Gavilan CG, Ventura M et al: Impact of Prematurity and Perinatal Antibiotics on the Developing Intestinal Microbiota: A Functional Inference Study. Int J Mol Sci 2016, 17(5).PubMedCentralCrossRef
31.
32.
go back to reference Liu L, Zhao H, Zhang Y, Wang J, Che Y, Dong C, Zhang X, Na R, Shi H, Jiang L, et al. Neonatal rhesus monkey is a potential animal model for studying pathogenesis of EV71 infection. Virology. 2011;412(1):91–100.PubMedCrossRef Liu L, Zhao H, Zhang Y, Wang J, Che Y, Dong C, Zhang X, Na R, Shi H, Jiang L, et al. Neonatal rhesus monkey is a potential animal model for studying pathogenesis of EV71 infection. Virology. 2011;412(1):91–100.PubMedCrossRef
33.
go back to reference Marx PA, Maul DH, Osborn KG, Lerche NW, Moody P, Lowenstine LJ, Henrickson RV, Arthur LO, Gilden RV, Gravell M, et al. Simian AIDS: isolation of a type D retrovirus and transmission of the disease. Science. 1984;223(4640):1083–6.PubMedCrossRef Marx PA, Maul DH, Osborn KG, Lerche NW, Moody P, Lowenstine LJ, Henrickson RV, Arthur LO, Gilden RV, Gravell M, et al. Simian AIDS: isolation of a type D retrovirus and transmission of the disease. Science. 1984;223(4640):1083–6.PubMedCrossRef
34.
go back to reference Zhang XX, Wu QF, Yan YL, Zhang FL. Inhibitory effects and related molecular mechanisms of total flavonoids in Mosla chinensis maxim against H1N1 influenza virus. Inflamm Res. 2018;67(2):179–89.PubMedCrossRef Zhang XX, Wu QF, Yan YL, Zhang FL. Inhibitory effects and related molecular mechanisms of total flavonoids in Mosla chinensis maxim against H1N1 influenza virus. Inflamm Res. 2018;67(2):179–89.PubMedCrossRef
35.
go back to reference Majmudar H, Hao M, Sankaranarayanan NV, Zanotti B, Volin MV, Desai UR, Tiwari V. A synthetic glycosaminoglycan mimetic blocks HSV-1 infection in human iris stromal cells. Antivir Res. 2018;161:154–62.PubMedCrossRef Majmudar H, Hao M, Sankaranarayanan NV, Zanotti B, Volin MV, Desai UR, Tiwari V. A synthetic glycosaminoglycan mimetic blocks HSV-1 infection in human iris stromal cells. Antivir Res. 2018;161:154–62.PubMedCrossRef
36.
go back to reference Greseth MD, Traktman P. De novo fatty acid biosynthesis contributes significantly to establishment of a bioenergetically favorable environment for vaccinia virus infection. PLoS Pathog. 2014;10(3):e1004021.PubMedPubMedCentralCrossRef Greseth MD, Traktman P. De novo fatty acid biosynthesis contributes significantly to establishment of a bioenergetically favorable environment for vaccinia virus infection. PLoS Pathog. 2014;10(3):e1004021.PubMedPubMedCentralCrossRef
37.
go back to reference Lieberherr C, Zhang G, Grafen A, Singethan K, Kendl S, Vogt V, Maier J, Bringmann G, Schneider-Schaulies J. The plant-derived naphthoquinone Droserone inhibits in vitro measles virus infection. Planta Med. 2017;83(3–04):232–8.PubMed Lieberherr C, Zhang G, Grafen A, Singethan K, Kendl S, Vogt V, Maier J, Bringmann G, Schneider-Schaulies J. The plant-derived naphthoquinone Droserone inhibits in vitro measles virus infection. Planta Med. 2017;83(3–04):232–8.PubMed
38.
go back to reference Agus A, Planchais J, Sokol H. Gut microbiota regulation of tryptophan metabolism in health and disease. Cell Host Microbe. 2018;23(6):716–24.CrossRefPubMed Agus A, Planchais J, Sokol H. Gut microbiota regulation of tryptophan metabolism in health and disease. Cell Host Microbe. 2018;23(6):716–24.CrossRefPubMed
39.
go back to reference Stehle T, Peters T, Hartmann L, Schelhaas M: Glycans controlling virus infections: meeting report on the 1st international symposium on Glycovirology Schontal, Germany, 02(−)04. Viruses 2018. May 2018:10(11). Stehle T, Peters T, Hartmann L, Schelhaas M: Glycans controlling virus infections: meeting report on the 1st international symposium on Glycovirology Schontal, Germany, 02(−)04. Viruses 2018. May 2018:10(11).
40.
go back to reference Lin LT, Chen TY, Lin SC, Chung CY, Lin TC, Wang GH, Anderson R, Lin CC, Richardson CD. Broad-spectrum antiviral activity of chebulagic acid and punicalagin against viruses that use glycosaminoglycans for entry. BMC Microbiol. 2013;13:187.PubMedPubMedCentralCrossRef Lin LT, Chen TY, Lin SC, Chung CY, Lin TC, Wang GH, Anderson R, Lin CC, Richardson CD. Broad-spectrum antiviral activity of chebulagic acid and punicalagin against viruses that use glycosaminoglycans for entry. BMC Microbiol. 2013;13:187.PubMedPubMedCentralCrossRef
41.
go back to reference Min BS, Miyashiro H, Hattori M. Inhibitory effects of quinones on RNase H activity associated with HIV-1 reverse transcriptase. Phytother Res. 2002;16(Suppl 1):S57–62.PubMedCrossRef Min BS, Miyashiro H, Hattori M. Inhibitory effects of quinones on RNase H activity associated with HIV-1 reverse transcriptase. Phytother Res. 2002;16(Suppl 1):S57–62.PubMedCrossRef
43.
go back to reference Arakawa T, Kita Y, Koyama AH. Synergistic virus inactivation effects of arginine. Biotechnol J. 2009;4(2):174–8.PubMedCrossRef Arakawa T, Kita Y, Koyama AH. Synergistic virus inactivation effects of arginine. Biotechnol J. 2009;4(2):174–8.PubMedCrossRef
44.
go back to reference Rabbani MAG, Barik S. 5-Hydroxytryptophan, a major product of tryptophan degradation, is essential for optimal replication of human parainfluenza virus. Virology. 2017;503:46–51.PubMedCrossRef Rabbani MAG, Barik S. 5-Hydroxytryptophan, a major product of tryptophan degradation, is essential for optimal replication of human parainfluenza virus. Virology. 2017;503:46–51.PubMedCrossRef
45.
go back to reference Drewes JL, Croteau JD, Shirk EN, Engle EL, Zink MC, Graham DR. Distinct patterns of tryptophan maintenance in tissues during kynurenine pathway activation in simian immunodeficiency virus-infected macaques. Front Immunol. 2016;7:605.PubMedPubMedCentralCrossRef Drewes JL, Croteau JD, Shirk EN, Engle EL, Zink MC, Graham DR. Distinct patterns of tryptophan maintenance in tissues during kynurenine pathway activation in simian immunodeficiency virus-infected macaques. Front Immunol. 2016;7:605.PubMedPubMedCentralCrossRef
46.
go back to reference Howe A, Ringus DL, Williams RJ, Choo ZN, Greenwald SM, Owens SM, Coleman ML, Meyer F, Chang EB. Divergent responses of viral and bacterial communities in the gut microbiome to dietary disturbances in mice. ISME J. 2016;10(5):1217–27.PubMedCrossRef Howe A, Ringus DL, Williams RJ, Choo ZN, Greenwald SM, Owens SM, Coleman ML, Meyer F, Chang EB. Divergent responses of viral and bacterial communities in the gut microbiome to dietary disturbances in mice. ISME J. 2016;10(5):1217–27.PubMedCrossRef
47.
go back to reference Yatsunenko T, Rey FE, Manary MJ, Trehan I, Dominguez-Bello MG, Contreras M, Magris M, Hidalgo G, Baldassano RN, Anokhin AP, et al. Human gut microbiome viewed across age and geography. Nature. 2012;486(7402):222–7.PubMedPubMedCentralCrossRef Yatsunenko T, Rey FE, Manary MJ, Trehan I, Dominguez-Bello MG, Contreras M, Magris M, Hidalgo G, Baldassano RN, Anokhin AP, et al. Human gut microbiome viewed across age and geography. Nature. 2012;486(7402):222–7.PubMedPubMedCentralCrossRef
48.
go back to reference Morgun A, Dzutsev A, Dong X, Greer RL, Sexton DJ, Ravel J, Schuster M, Hsiao W, Matzinger P, Shulzhenko N. Uncovering effects of antibiotics on the host and microbiota using transkingdom gene networks. Gut. 2015;64(11):1732–43.PubMedCrossRef Morgun A, Dzutsev A, Dong X, Greer RL, Sexton DJ, Ravel J, Schuster M, Hsiao W, Matzinger P, Shulzhenko N. Uncovering effects of antibiotics on the host and microbiota using transkingdom gene networks. Gut. 2015;64(11):1732–43.PubMedCrossRef
49.
go back to reference Xiong W, Wang Y, Sun Y, Ma L, Zeng Q, Jiang X, Li A, Zeng Z, Zhang T. Antibiotic-mediated changes in the fecal microbiome of broiler chickens define the incidence of antibiotic resistance genes. Microbiome. 2018;6(1):34.PubMedPubMedCentralCrossRef Xiong W, Wang Y, Sun Y, Ma L, Zeng Q, Jiang X, Li A, Zeng Z, Zhang T. Antibiotic-mediated changes in the fecal microbiome of broiler chickens define the incidence of antibiotic resistance genes. Microbiome. 2018;6(1):34.PubMedPubMedCentralCrossRef
50.
go back to reference Sharland M, Subgroup SP. The use of antibacterials in children: a report of the specialist advisory committee on antimicrobial resistance (SACAR) Paediatric Subgroup. J Antimicrob Chemother. 2007;60(Suppl 1):i15–26.PubMedCrossRef Sharland M, Subgroup SP. The use of antibacterials in children: a report of the specialist advisory committee on antimicrobial resistance (SACAR) Paediatric Subgroup. J Antimicrob Chemother. 2007;60(Suppl 1):i15–26.PubMedCrossRef
51.
go back to reference Lai YC, Chuang YC, Chang CP, Lin YS, Perng GC, Wu HC, Hsieh SL, Yeh TM. Minocycline suppresses dengue virus replication by down-regulation of macrophage migration inhibitory factor-induced autophagy. Antivir Res. 2018;155:28–38.PubMedCrossRef Lai YC, Chuang YC, Chang CP, Lin YS, Perng GC, Wu HC, Hsieh SL, Yeh TM. Minocycline suppresses dengue virus replication by down-regulation of macrophage migration inhibitory factor-induced autophagy. Antivir Res. 2018;155:28–38.PubMedCrossRef
52.
go back to reference Varghese FS, Kaukinen P, Glasker S, Bespalov M, Hanski L, Wennerberg K, Kummerer BM, Ahola T. Discovery of berberine, abamectin and ivermectin as antivirals against chikungunya and other alphaviruses. Antivir Res. 2016;126:117–24.PubMedCrossRef Varghese FS, Kaukinen P, Glasker S, Bespalov M, Hanski L, Wennerberg K, Kummerer BM, Ahola T. Discovery of berberine, abamectin and ivermectin as antivirals against chikungunya and other alphaviruses. Antivir Res. 2016;126:117–24.PubMedCrossRef
53.
go back to reference Zhou N, Pan T, Zhang J, Li Q, Zhang X, Bai C, Huang F, Peng T, Zhang J, Liu C, et al. Glycopeptide antibiotics potently inhibit Cathepsin L in the late endosome/lysosome and block the entry of Ebola virus, Middle East respiratory syndrome coronavirus (MERS-CoV), and severe acute respiratory syndrome coronavirus (SARS-CoV). J Biol Chem. 2016;291(17):9218–32.PubMedPubMedCentralCrossRef Zhou N, Pan T, Zhang J, Li Q, Zhang X, Bai C, Huang F, Peng T, Zhang J, Liu C, et al. Glycopeptide antibiotics potently inhibit Cathepsin L in the late endosome/lysosome and block the entry of Ebola virus, Middle East respiratory syndrome coronavirus (MERS-CoV), and severe acute respiratory syndrome coronavirus (SARS-CoV). J Biol Chem. 2016;291(17):9218–32.PubMedPubMedCentralCrossRef
54.
go back to reference De Burghgraeve T, Kaptein SJ, Ayala-Nunez NV, Mondotte JA, Pastorino B, Printsevskaya SS, de Lamballerie X, Jacobs M, Preobrazhenskaya M, Gamarnik AV, et al. An analogue of the antibiotic teicoplanin prevents flavivirus entry in vitro. PLoS One. 2012;7(5):e37244.PubMedPubMedCentralCrossRef De Burghgraeve T, Kaptein SJ, Ayala-Nunez NV, Mondotte JA, Pastorino B, Printsevskaya SS, de Lamballerie X, Jacobs M, Preobrazhenskaya M, Gamarnik AV, et al. An analogue of the antibiotic teicoplanin prevents flavivirus entry in vitro. PLoS One. 2012;7(5):e37244.PubMedPubMedCentralCrossRef
55.
go back to reference Finkbeiner SR, Allred AF, Tarr PI, Klein EJ, Kirkwood CD, Wang D. Metagenomic analysis of human diarrhea: viral detection and discovery. PLoS Pathog. 2008;4(2):e1000011.PubMedPubMedCentralCrossRef Finkbeiner SR, Allred AF, Tarr PI, Klein EJ, Kirkwood CD, Wang D. Metagenomic analysis of human diarrhea: viral detection and discovery. PLoS Pathog. 2008;4(2):e1000011.PubMedPubMedCentralCrossRef
56.
go back to reference Morse SS, Mazet JA, Woolhouse M, Parrish CR, Carroll D, Karesh WB, Zambrana-Torrelio C, Lipkin WI, Daszak P. Prediction and prevention of the next pandemic zoonosis. Lancet. 2012;380(9857):1956–65.PubMedPubMedCentralCrossRef Morse SS, Mazet JA, Woolhouse M, Parrish CR, Carroll D, Karesh WB, Zambrana-Torrelio C, Lipkin WI, Daszak P. Prediction and prevention of the next pandemic zoonosis. Lancet. 2012;380(9857):1956–65.PubMedPubMedCentralCrossRef
Metadata
Title
The altered gut virome community in rhesus monkeys is correlated with the gut bacterial microbiome and associated metabolites
Authors
Heng Li
Hongzhe Li
Jingjing Wang
Lei Guo
Haitao Fan
Huiwen Zheng
Zening Yang
Xing Huang
Manman Chu
Fengmei Yang
Zhanlong He
Nan Li
Jinxi Yang
Qiongwen Wu
Haijing Shi
Longding Liu
Publication date
01-12-2019
Publisher
BioMed Central
Keyword
Antibiotic
Published in
Virology Journal / Issue 1/2019
Electronic ISSN: 1743-422X
DOI
https://doi.org/10.1186/s12985-019-1211-z

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