The Human Gut Phageome: Origins and Roles in the Human Gut Microbiome.

Eleanor M Townsend, Lucy Kelly, George Muscatt, Joshua D Box, Nicole Hargraves, Daniel Lilley, Eleanor Jameson
Author Information
  1. Eleanor M Townsend: School of Life Sciences, The University of Warwick, Coventry, United Kingdom.
  2. Lucy Kelly: School of Life Sciences, The University of Warwick, Coventry, United Kingdom.
  3. George Muscatt: School of Life Sciences, The University of Warwick, Coventry, United Kingdom.
  4. Joshua D Box: School of Life Sciences, The University of Warwick, Coventry, United Kingdom.
  5. Nicole Hargraves: School of Life Sciences, The University of Warwick, Coventry, United Kingdom.
  6. Daniel Lilley: Warwick Medical School, The University of Warwick, Coventry, United Kingdom.
  7. Eleanor Jameson: School of Life Sciences, The University of Warwick, Coventry, United Kingdom.

Abstract

The investigation of the microbial populations of the Human body, known as the microbiome, has led to a revolutionary field of science, and understanding of its impacts on Human development and health. The majority of microbiome research to date has focussed on bacteria and other kingdoms of life, such as fungi. Trailing behind these is the interrogation of the gut viruses, specifically the phageome. bacteriophages, viruses that infect bacterial hosts, are known to dictate the dynamics and diversity of bacterial populations in a number of ecosystems. However, the phageome of the Human gut, while of apparent importance, remains an area of many unknowns. In this paper we discuss the role of bacteriophages within the Human gut microbiome. We examine the methods used to study bacteriophage populations, how this evolved over time and what we now understand about the phageome. We review the phageome development in infancy, and factors that may influence phage populations in adult life. The role and action of the phageome is then discussed at both a biological-level, and in the broader context of Human health and disease.

Keywords

References

  1. mBio. 2011 Nov 29;2(6): [PMID: 22128350]
  2. Microbiome. 2018 Apr 10;6(1):68 [PMID: 29631623]
  3. Nat Microbiol. 2016 Nov 07;1:16203 [PMID: 27819657]
  4. Front Microbiol. 2014 Jul 17;5:361 [PMID: 25101067]
  5. Front Microbiol. 2018 Jun 01;9:1162 [PMID: 29910789]
  6. Proc Natl Acad Sci U S A. 2012 Mar 6;109(10):3962-6 [PMID: 22355105]
  7. Nat Med. 2006 Dec;12(12):1365-71 [PMID: 17115046]
  8. Trends Microbiol. 2013 Jan;21(1):1-5 [PMID: 23140888]
  9. Nucleic Acids Res. 2019 Jan 8;47(D1):D427-D432 [PMID: 30357350]
  10. J Bacteriol. 1996 Apr;178(7):2044-50 [PMID: 8606182]
  11. PLoS Biol. 2006 Jan;4(1):e3 [PMID: 16336043]
  12. Virology. 2006 Jun 20;350(1):146-57 [PMID: 16643978]
  13. Cell Host Microbe. 2019 Feb 13;25(2):195-209 [PMID: 30763534]
  14. Nat Commun. 2017 Jun 23;8:15892 [PMID: 28643787]
  15. Appl Microbiol Biotechnol. 2016 Mar;100(5):2141-51 [PMID: 26767986]
  16. Sci Rep. 2017 Aug 1;7(1):7043 [PMID: 28765534]
  17. Sci Rep. 2015 Nov 12;5:16532 [PMID: 26559140]
  18. Microbiome. 2017 Nov 25;5(1):153 [PMID: 29178920]
  19. Nutr Today. 2015 Jul;50(4):189-193 [PMID: 27340300]
  20. PLoS Pathog. 2015 Feb 23;11(2):e1004653 [PMID: 25706310]
  21. ISME J. 2014 Jul;8(7):1391-402 [PMID: 24621522]
  22. J Appl Microbiol. 2014 Sep;117(3):627-33 [PMID: 24916438]
  23. Microbiome. 2018 Apr 3;6(1):65 [PMID: 29615108]
  24. Nucleic Acids Res. 2021 Jan 8;49(D1):D764-D775 [PMID: 33137183]
  25. Viruses. 2018 Jul 21;10(7): [PMID: 30037084]
  26. Methods Mol Biol. 2009;501:55-66 [PMID: 19066810]
  27. Virol J. 2019 Aug 19;16(1):105 [PMID: 31426820]
  28. J Bacteriol. 2008 Feb;190(4):1390-400 [PMID: 18065545]
  29. J Pediatr Gastroenterol Nutr. 2019 Jan;68(1):30-36 [PMID: 30169455]
  30. J Appl Microbiol. 2007 May;102(5):1187-96 [PMID: 17448154]
  31. Microbiome. 2017 Jun 26;5(1):66 [PMID: 28651630]
  32. Bacteriophage. 2012 Jul 1;2(3):149-158 [PMID: 23275866]
  33. PeerJ. 2018 May 7;6:e4694 [PMID: 29761040]
  34. Nat Protoc. 2015 Jun;10(6):845-58 [PMID: 25950237]
  35. Allergol Int. 2017 Oct;66(4):515-522 [PMID: 28826938]
  36. Brain Behav Immun. 2017 May;62:46-52 [PMID: 28003152]
  37. EBioMedicine. 2016 Jan 05;4:124-37 [PMID: 26981577]
  38. Curr Opin Virol. 2012 Feb;2(1):63-77 [PMID: 22440968]
  39. Cell Host Microbe. 2019 Feb 13;25(2):285-299.e8 [PMID: 30763538]
  40. PLoS One. 2020 Jan 15;15(1):e0226930 [PMID: 31940321]
  41. Antimicrob Agents Chemother. 2014;58(1):606-9 [PMID: 24165177]
  42. Nat Commun. 2018 Nov 14;9(1):4781 [PMID: 30429469]
  43. Microbiome. 2018 Feb 01;6(1):24 [PMID: 29391057]
  44. Immunity. 2019 Apr 16;50(4):941-954 [PMID: 30995508]
  45. J Cyst Fibros. 2013 Mar;12(2):154-64 [PMID: 22951208]
  46. Proc Natl Acad Sci U S A. 2013 Jul 23;110(30):12450-5 [PMID: 23836644]
  47. Cell Host Microbe. 2013 Jul 17;14(1):26-37 [PMID: 23870311]
  48. Mol Biol Evol. 2013 Apr;30(4):772-80 [PMID: 23329690]
  49. Inflamm Bowel Dis. 2012 Oct;18(10):1799-808 [PMID: 22170749]
  50. FEMS Immunol Med Microbiol. 2006 Apr;46(3):313-9 [PMID: 16553803]
  51. Proc Natl Acad Sci U S A. 2009 Jan 20;106(3):894-9 [PMID: 19124776]
  52. Am J Gastroenterol. 2011 Apr;106(4):741-7 [PMID: 21386828]
  53. Appl Environ Microbiol. 1995 Sep;61(9):3227-31 [PMID: 7574632]
  54. Mediators Inflamm. 2015;2015:326032 [PMID: 25944980]
  55. Antibiotics (Basel). 2018 Feb 13;7(1): [PMID: 29438355]
  56. Cell Host Microbe. 2018 Nov 14;24(5):653-664.e6 [PMID: 30449316]
  57. mBio. 2010 Aug 24;1(3): [PMID: 20824103]
  58. Nat Rev Microbiol. 2016 Jan;14(1):20-32 [PMID: 26499895]
  59. Nat Med. 2015 Oct;21(10):1228-34 [PMID: 26366711]
  60. ISME J. 2009 Mar;3(3):271-82 [PMID: 19005496]
  61. BMC Genomics. 2014 Jan 18;15:37 [PMID: 24438450]
  62. Nature. 2004 Sep 23;431(7007):476-81 [PMID: 15386016]
  63. BMC Genomics. 2015 Jan 22;16:7 [PMID: 25608871]
  64. Proc Natl Acad Sci U S A. 2015 Sep 22;112(38):11941-6 [PMID: 26351661]
  65. Appl Environ Microbiol. 2003 Jun;69(6):3192-202 [PMID: 12788716]
  66. Front Microbiol. 2016 Jul 14;7:1112 [PMID: 27471503]
  67. ISME J. 2017 Jan;11(1):237-247 [PMID: 27326545]
  68. New Biol. 1991 Mar;3(3):230-6 [PMID: 1831658]
  69. Microbiol Mol Biol Rev. 2000 Mar;64(1):69-114 [PMID: 10704475]
  70. PLoS One. 2013;8(4):e60621 [PMID: 23573274]
  71. J Med Microbiol. 2005 Oct;54(Pt 10):987-991 [PMID: 16157555]
  72. mBio. 2017 Nov 21;8(6): [PMID: 29162715]
  73. Clin Microbiol Infect. 2012 Dec;18(12):1185-93 [PMID: 23033984]
  74. J Infect Dis. 2015 Jan 1;211(1):19-27 [PMID: 25057045]
  75. Dis Model Mech. 2015 Jan;8(1):1-16 [PMID: 25561744]
  76. Nat Biotechnol. 2021 May;39(5):578-585 [PMID: 33349699]
  77. Annu Rev Microbiol. 1987;41:435-64 [PMID: 3318676]
  78. Nucleic Acids Res. 2017 Jan 4;45(D1):D491-D498 [PMID: 27789703]
  79. Proc Natl Acad Sci U S A. 2017 Jul 25;114(30):E6166-E6175 [PMID: 28696303]
  80. J Bacteriol. 2008 Sep;190(17):5806-13 [PMID: 18515417]
  81. Nat Commun. 2020 Jan 15;11(1):280 [PMID: 31941900]
  82. Inflamm Bowel Dis. 2013 Jul;19(8):1598-608 [PMID: 23749273]
  83. Trends Microbiol. 2016 Oct;24(10):801-810 [PMID: 27353648]
  84. Proc Natl Acad Sci U S A. 2013 Jun 25;110(26):10771-6 [PMID: 23690590]
  85. PLoS One. 2010 Apr 06;5(4):e10041 [PMID: 20386604]
  86. Int J Microbiol. 2012;2012:863945 [PMID: 23316235]
  87. Viruses. 2018 Apr 19;10(4): [PMID: 29671810]
  88. Trends Microbiol. 1994 Apr;2(4):137-9 [PMID: 8012757]
  89. Cell Host Microbe. 2019 Jun 12;25(6):803-814.e5 [PMID: 31175044]
  90. J Bacteriol. 2003 Aug;185(15):4603-8 [PMID: 12867471]
  91. Nutr Healthy Aging. 2018 Jun 15;4(4):267-285 [PMID: 29951588]
  92. Appl Environ Microbiol. 2014 Jun;80(11):3508-17 [PMID: 24682298]
  93. Nature. 2010 Mar 4;464(7285):59-65 [PMID: 20203603]
  94. Comput Struct Biotechnol J. 2015 Jun 09;13:390-401 [PMID: 26137199]
  95. Gastroenterology. 2014 May;146(6):1459-69 [PMID: 24508599]
  96. Microbiome. 2017 Jan 23;5(1):10 [PMID: 28122648]
  97. J Food Prot. 1984 Aug;47(8):623-626 [PMID: 30934401]
  98. Asian-Australas J Anim Sci. 2012 Jul;25(7):1015-20 [PMID: 25049658]
  99. Water Res. 2015 Jan 1;68:414-22 [PMID: 25462748]
  100. Microbiology (Reading). 2010 Nov;156(Pt 11):3216-3223 [PMID: 20705661]
  101. Nucleic Acids Res. 2020 Sep 18;48(16):8883-8900 [PMID: 32766782]
  102. Cell Host Microbe. 2016 Mar 9;19(3):311-22 [PMID: 26962942]
  103. Cell Host Microbe. 2019 Feb 13;25(2):219-232 [PMID: 30763536]
  104. Microb Ecol Health Dis. 2015 Mar 12;26:26914 [PMID: 25769266]
  105. Gut. 2018 Apr;67(4):634-643 [PMID: 28539351]
  106. ISME J. 2012 Jul;6(7):1415-26 [PMID: 22258098]
  107. Viruses. 2017 May 24;9(6): [PMID: 28538703]
  108. Res Microbiol. 2008 Jun;159(5):367-73 [PMID: 18541415]
  109. J Gen Virol. 1983 Sep;64 (Pt 9):2039-43 [PMID: 6886680]
  110. Sci Rep. 2017 Jan 04;7:39642 [PMID: 28051127]
  111. Microbiome. 2015 Nov 17;3:64 [PMID: 26577924]
  112. J Bacteriol. 1978 Mar;133(3):1144-9 [PMID: 147865]
  113. Trends Microbiol. 2019 Jan;27(1):17-25 [PMID: 30219265]
  114. J Am Coll Cardiol. 2007 Oct 16;50(16):1561-9 [PMID: 17936155]
  115. Chem Biodivers. 2010 May;7(5):1065-75 [PMID: 20491064]
  116. Nature. 2014 Jan 23;505(7484):559-63 [PMID: 24336217]
  117. CNS Drugs. 2016 Nov;30(11):1019-1041 [PMID: 27417321]
  118. Nat Rev Microbiol. 2019 Dec;17(12):764-775 [PMID: 31417197]
  119. Appl Environ Microbiol. 2018 Aug 17;84(17): [PMID: 29915115]
  120. AIDS. 2016 Nov 28;30(18):2737-2751 [PMID: 27755100]
  121. ISME J. 2018 Apr;12(4):1127-1141 [PMID: 29416123]
  122. Nat Microbiol. 2019 Dec;4(12):2192-2203 [PMID: 31384000]
  123. Sci Total Environ. 2020 Sep 10;734:139424 [PMID: 32464399]
  124. Proc Natl Acad Sci U S A. 2019 Dec 17;116(51):25900-25908 [PMID: 31772013]
  125. Front Microbiol. 2015 Nov 13;6:1271 [PMID: 26617601]
  126. Inflamm Bowel Dis. 2005 May;11(5):473-80 [PMID: 15867587]
  127. Gastroenterology. 2017 Mar;152(4):799-811.e7 [PMID: 27866880]
  128. Nat Microbiol. 2019 Apr;4(4):693-700 [PMID: 30692672]
  129. PLoS One. 2015 Aug 26;10(8):e0134941 [PMID: 26309137]
  130. Biomol Concepts. 2018 Nov 23;9(1):131-142 [PMID: 30481150]
  131. BMC Biol. 2020 Nov 20;18(1):173 [PMID: 33218339]
  132. Bioinformatics. 2019 Nov 1;35(22):4537-4542 [PMID: 31329826]
  133. Antimicrob Agents Chemother. 2005 Jul;49(7):2874-8 [PMID: 15980363]
  134. Nature. 2013 Jul 11;499(7457):219-22 [PMID: 23748443]
  135. Front Microbiol. 2016 Apr 20;7:459 [PMID: 27148170]
  136. J Appl Microbiol. 1997 Nov;83(5):627-33 [PMID: 9418024]
  137. Res Microbiol. 2014 Dec;165(10):803-12 [PMID: 25463385]
  138. Water Sci Technol. 2010;61(2):293-300 [PMID: 20107254]
  139. Bacteriophage. 2013 Jul 1;3(3):e25857 [PMID: 24228227]
  140. Nat Rev Microbiol. 2017 Jul;15(7):397-408 [PMID: 28461690]
  141. Biotechnol Bioeng. 2010 Mar 1;105(4):678-86 [PMID: 19891006]
  142. Appl Environ Microbiol. 2014 Aug;80(15):4470-80 [PMID: 24837394]
  143. J Bacteriol. 1973 Mar;113(3):1491-504 [PMID: 4120609]
  144. PLoS Pathog. 2014 Jul 31;10(7):e1004219 [PMID: 25078987]
  145. Mucosal Immunol. 2015 Sep;8(5):1009-20 [PMID: 25586559]
  146. Nat Commun. 2013;4:2420 [PMID: 24036533]
  147. Nat Methods. 2009 Sep;6(9):673-6 [PMID: 19648916]
  148. Gut. 2019 Jul;68(7):1169-1179 [PMID: 30842211]
  149. Virology. 2019 Jan 15;527:77-88 [PMID: 30468938]
  150. Nat Commun. 2014 Jul 24;5:4498 [PMID: 25058116]
  151. Nature. 2012 Oct 4;490(7418):55-60 [PMID: 23023125]
  152. Nature. 2020 May;581(7809):470-474 [PMID: 32461640]
  153. Proc Natl Acad Sci U S A. 2016 Jul 19;113(29):8266-71 [PMID: 27382184]
  154. Diabetes Care. 2009 Jan;32 Suppl 1:S62-7 [PMID: 19118289]
  155. Proc Natl Acad Sci U S A. 2012 Oct 23;109(43):17621-6 [PMID: 23045666]
  156. Nat Rev Genet. 2008 Apr;9(4):267-76 [PMID: 18319742]
  157. Nature. 2018 Feb 1;554(7690):118-122 [PMID: 29364876]
  158. J Food Prot. 2002 Oct;65(10):1597-604 [PMID: 12380745]
  159. Genome Res. 2012 Oct;22(10):1985-94 [PMID: 22732228]
  160. J Bacteriol. 2011 Dec;193(23):6742-9 [PMID: 21965558]
  161. Science. 2017 Mar 17;355(6330):1211-1215 [PMID: 28302859]
  162. Inflamm Bowel Dis. 2015 Nov;21(11):2515-32 [PMID: 26313691]
  163. Mob Genet Elements. 2013 Jul 1;3(4):e25847 [PMID: 24195016]
  164. Nat Microbiol. 2018 Jan;3(1):90-98 [PMID: 29085076]
  165. Proc Natl Acad Sci U S A. 2000 May 23;97(11):5995-6000 [PMID: 10801973]
  166. J Clin Pathol. 1974 Aug;27(8):603-8 [PMID: 4138653]
  167. Trends Microbiol. 2016 Jun;24(6):503-513 [PMID: 27004827]
  168. Microbiome. 2017 Jul 6;5(1):69 [PMID: 28683828]
  169. Inflamm Bowel Dis. 2010 Dec;16(12):2034-42 [PMID: 20848492]
  170. Appl Environ Microbiol. 2012 Oct;78(20):7299-308 [PMID: 22885743]
  171. Appl Environ Microbiol. 2002 Feb;68(2):973-6 [PMID: 11823247]
  172. Front Endocrinol (Lausanne). 2019 Nov 29;10:784 [PMID: 31849833]
  173. PLoS One. 2008 Jan 23;3(1):e1456 [PMID: 18213365]
  174. EMBO J. 2015 Jan 13;34(2):169-83 [PMID: 25452498]
  175. PLoS Comput Biol. 2011 Oct;7(10):e1002195 [PMID: 22039361]
  176. Nat Rev Microbiol. 2010 Sep;8(9):623-33 [PMID: 20676145]
  177. Front Microbiol. 2014 Dec 23;5:724 [PMID: 25566233]
  178. Clin Microbiol Rev. 2015 Jan;28(1):237-64 [PMID: 25567229]
  179. Nature. 2012 Sep 13;489(7415):220-30 [PMID: 22972295]
  180. PLoS One. 2014 Aug 20;9(8):e105067 [PMID: 25140992]
  181. Cell Host Microbe. 2020 Nov 11;28(5):724-740.e8 [PMID: 32841606]
  182. Cell. 2015 Jan 29;160(3):447-60 [PMID: 25619688]
  183. J Food Prot. 1986 Dec;49(12):944-951 [PMID: 30965462]
  184. Nat Microbiol. 2018 Jan;3(1):38-46 [PMID: 29133882]
  185. Quant Biol. 2020 Mar;8(1):64-77 [PMID: 34084563]
  186. Microbiome. 2021 Feb 1;9(1):37 [PMID: 33522966]
  187. J Water Health. 2004 Sep;2(3):201-14 [PMID: 15497816]
  188. Virol J. 2019 Dec 12;16(1):155 [PMID: 31831017]
  189. Inflamm Bowel Dis. 2006 Dec;12(12):1136-45 [PMID: 17119388]
  190. J Bacteriol. 1995 Jun;177(11):3080-6 [PMID: 7768804]
  191. Res Microbiol. 2011 Oct;162(8):737-46 [PMID: 21767638]
  192. FEMS Microbiol Lett. 1998 Nov 1;168(1):119-25 [PMID: 9812372]
  193. Nat Commun. 2019 Mar 12;10(1):1169 [PMID: 30862830]
  194. Mob DNA. 2017 Oct 3;8:12 [PMID: 29026445]
  195. Trends Microbiol. 2016 Nov;24(11):887-901 [PMID: 27426971]
  196. Clin Microbiol Infect. 2012 Nov;18(11):1126-33 [PMID: 22084916]
  197. Proc Natl Acad Sci U S A. 2013 Dec 10;110(50):20236-41 [PMID: 24259713]
  198. Sci Transl Med. 2016 Jun 15;8(343):343ra81 [PMID: 27306663]
  199. Nat Microbiol. 2018 Sep;3(9):1023-1031 [PMID: 30038310]
  200. FEBS Lett. 2009 Jun 18;583(12):2100-7 [PMID: 19481546]
  201. Pediatr Diabetes. 2017 Nov;18(7):588-598 [PMID: 27860030]
  202. PLoS Biol. 2016 Jul 12;14(7):e1002503 [PMID: 27404502]
  203. Cell. 2021 Feb 18;184(4):1098-1109.e9 [PMID: 33606979]
  204. Cell Host Microbe. 2014 Jan 15;15(1):47-57 [PMID: 24439897]
  205. PLoS Biol. 2016 Aug 19;14(8):e1002533 [PMID: 27541692]
  206. J Exp Med. 2019 Jan 7;216(1):20-40 [PMID: 30322864]
  207. mSphere. 2020 Feb 26;5(1): [PMID: 32102942]
  208. F1000Res. 2019 Jul 1;8: [PMID: 31316751]
  209. Nature. 2010 Jul 15;466(7304):334-8 [PMID: 20631792]
  210. Nat Microbiol. 2018 Jul;3(7):754-766 [PMID: 29867096]
  211. Gut. 2008 Mar;57(3):424-5 [PMID: 18268057]
  212. Proc Natl Acad Sci U S A. 2016 Sep 13;113(37):10400-5 [PMID: 27573828]
  213. Sci Rep. 2019 Jul 4;9(1):9685 [PMID: 31273267]
  214. Gut Microbes. 2019;10(1):92-99 [PMID: 29913091]
  215. J Bacteriol. 2003 Oct;185(20):6220-3 [PMID: 14526037]
  216. NPJ Biofilms Microbiomes. 2016 Jul 06;2:16010 [PMID: 28721247]
  217. J Pediatr. 2003 Dec;143(6):754-8 [PMID: 14657823]
  218. Genome Res. 2013 Jan;23(1):111-20 [PMID: 22936250]
  219. Genome Res. 2011 Oct;21(10):1616-25 [PMID: 21880779]
  220. PLoS One. 2014 Aug 18;9(8):e105221 [PMID: 25133738]
  221. J Gen Microbiol. 1976 Jul;95(1):166-72 [PMID: 784901]
  222. Eur J Cardiothorac Surg. 2020 May 1;57(5):1003-1004 [PMID: 31651936]
  223. Cell. 2006 Feb 24;124(4):837-48 [PMID: 16497592]
  224. Nature. 2011 Apr 7;472(7341):57-63 [PMID: 21475195]
  225. Int J Hyg Environ Health. 2002 May;205(4):325-8 [PMID: 12068752]
  226. Cell Immunol. 2015 Sep;297(1):33-9 [PMID: 26077826]
  227. Cell Host Microbe. 2019 Oct 9;26(4):527-541.e5 [PMID: 31600503]
  228. FEMS Microbiol Rev. 2014 Sep;38(5):916-31 [PMID: 24617569]
  229. Nat Biotechnol. 2014 Aug;32(8):834-41 [PMID: 24997786]
  230. Biochem J. 2005 Aug 1;389(Pt 3):869-76 [PMID: 15862112]
  231. J Food Prot. 2004 Nov;67(11):2387-90 [PMID: 15553617]
  232. BMC Bioinformatics. 2010 Mar 08;11:119 [PMID: 20211023]
  233. Sci Adv. 2020 Feb 07;6(6):eaay5981 [PMID: 32083183]
  234. Anaerobe. 2011 Apr;17(2):56-63 [PMID: 21420503]
  235. Curr Opin Microbiol. 2005 Aug;8(4):473-9 [PMID: 15979388]
  236. Front Microbiol. 2019 Jan 23;9:3328 [PMID: 30761120]
  237. Viruses. 2015 Aug 20;7(8):4783-99 [PMID: 26308042]
  238. Nat Protoc. 2009;4(4):470-83 [PMID: 19300441]
  239. ISME J. 2014 Aug;8(8):1566-76 [PMID: 24522263]
  240. J Gastroenterol. 2011 Apr;46(4):479-86 [PMID: 21253779]
  241. Nat Commun. 2010;1:147 [PMID: 21266997]
  242. Bacteriophage. 2015 Aug 28;5(4):e1088124 [PMID: 26909243]
  243. J Bacteriol. 2006 Apr;188(7):2726-9 [PMID: 16547063]
  244. Cell. 2012 Oct 12;151(2):253-66 [PMID: 23063120]
  245. Nat Rev Microbiol. 2012 Sep;10(9):607-17 [PMID: 22864264]
  246. Cell Host Microbe. 2019 Dec 11;26(6):764-778.e5 [PMID: 31757768]
  247. Open Virol J. 2012;6:91-6 [PMID: 23136622]
  248. J Clin Microbiol. 2005 Jul;43(7):3380-9 [PMID: 16000463]
  249. Gut Microbes. 2019;10(6):676-687 [PMID: 30866714]
  250. Front Microbiol. 2018 Dec 19;9:3150 [PMID: 30619215]
  251. Nature. 2011 Jun 15;474(7351):307-17 [PMID: 21677747]
  252. Bioinformatics. 2017 Oct 1;33(19):3113-3114 [PMID: 28957499]
  253. PLoS One. 2009 Aug 12;4(8):e6532 [PMID: 19672290]
  254. ISME J. 2016 May;10(5):1217-27 [PMID: 26473721]
  255. J Appl Microbiol. 1998 Sep;85(3):583-90 [PMID: 9750288]
  256. Appl Environ Microbiol. 2011 Nov;77(22):8062-70 [PMID: 21948823]
  257. Nucleic Acids Res. 2012 Jan;40(Database issue):D284-9 [PMID: 22096231]
  258. J Virol. 1974 Aug;14(2):198-202 [PMID: 4277011]
  259. Microbiology (Reading). 2017 Nov;163(11):1568-1577 [PMID: 28982395]
  260. Environ Microbiol. 2013 Aug;15(8):2306-18 [PMID: 23489642]
  261. BMC Med. 2016 Jun 03;14(1):83 [PMID: 27256449]
  262. Annu Rev Microbiol. 1980;34:137-58 [PMID: 7002022]
  263. PeerJ. 2017 Sep 21;5:e3817 [PMID: 28948103]
  264. Autoimmun Rev. 2018 Jul;17(7):703-708 [PMID: 29730525]
  265. J Dairy Sci. 2006 Oct;89(10):3791-9 [PMID: 16960053]
  266. Gut Pathog. 2016 Jun 23;8:33 [PMID: 27340433]
  267. Nat Commun. 2017 Oct 10;8(1):845 [PMID: 29018189]
  268. Mol Microbiol. 2006 Jun;60(5):1123-35 [PMID: 16689790]
  269. EMBO J. 1996 Mar 1;15(5):1028-36 [PMID: 8605872]
  270. Science. 2005 Jun 10;308(5728):1635-8 [PMID: 15831718]
  271. AIDS. 2008 Oct 1;22(15):2035-8 [PMID: 18784466]
  272. Bioinformatics. 2014 Jul 15;30(14):2068-9 [PMID: 24642063]
  273. Gut. 2020 Dec;69(12):2122-2130 [PMID: 32165408]
  274. BMC Bioinformatics. 2009 Dec 15;10:421 [PMID: 20003500]
  275. Gut Microbes. 2013 Jan-Feb;4(1):4-16 [PMID: 23022738]
  276. Front Microbiol. 2014 May 13;5:217 [PMID: 24860564]
  277. ISME J. 2019 Nov;13(11):2856-2867 [PMID: 31358910]
  278. J Transl Med. 2017 Apr 8;15(1):73 [PMID: 28388917]
  279. BMC Genomics. 2020 Feb 5;21(1):126 [PMID: 32024463]
  280. Nat Microbiol. 2016 Jun 13;1(8):16088 [PMID: 27573110]
  281. Am J Gastroenterol. 2008 Feb;103(2):397-8 [PMID: 18289202]
  282. Nat Microbiol. 2019 Oct;4(10):1727-1736 [PMID: 31285584]
  283. Proc Natl Acad Sci U S A. 2015 Nov 3;112(44):13675-80 [PMID: 26483471]
  284. Cell Host Microbe. 2020 Feb 12;27(2):199-212.e5 [PMID: 32053789]
  285. Curr Opin Microbiol. 2007 Aug;10(4):382-7 [PMID: 17765600]
  286. PLoS One. 2010 Dec 20;5(12):e15678 [PMID: 21187931]
  287. Elife. 2013 Dec 17;2:e01299 [PMID: 24347545]

Grants

  1. BB/M017982/1/Biotechnology and Biological Sciences Research Council

MeSH Term

Bacteria
Bacteriophages
Gastrointestinal Microbiome
Humans
Microbiota
Virome

Word Cloud

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