Skip to main content
SpringerLink
Log in

The Diversity of Bacteriophages in the Human Gut

  • Protocol
  • First Online:
Bacteriophages

Part of the book series: Methods in Molecular Biology ((MIMB,volume 2738))

Abstract

Bacteriophages, commonly referred to as phages, are viruses that infect bacteria and are among the most numerous microorganisms on the planet. They occur throughout nature occupying every habitat where their bacterial hosts can be found. Within these communities, phages are responsible for shaping the bacterial community structure and function through their interactions. Phages shape the community structure and function within the human gut but are also able to influence the human host. As such, there is increased interest in understanding the composition and activity of the gastrointestinal phages, although these studies have been hindered by the difficulties accompanying the study of the human gut. Here, we summarize the methods and findings pertaining to the diversity of the human gastrointestinal phages.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Protocol
USD 49.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  1. Clooney AG, Sutton TDS, Shkoporov AN, Holohan RK, Daly KM, O’Regan O, Ryan FJ, Draper LA, Plevy SE, Ross RP, Hill C (2019) Whole-Virome analysis sheds light on viral dark matter in inflammatory bowel disease. Cell Host Microbe 26(6):764–778 e765. https://doi.org/10.1016/j.chom.2019.10.009

  2. Laudadio I, Fulci V, Palone F, Stronati L, Cucchiara S, Carissimi C (2018) Quantitative assessment of shotgun metagenomics and 16S rDNA amplicon sequencing in the study of human gut microbiome. OMICS 22(4):248–254. https://doi.org/10.1089/omi.2018.0013

    Article  CAS  PubMed  Google Scholar 

  3. Liu YX, Qin Y, Chen T, Lu M, Qian X, Guo X, Bai Y (2021) A practical guide to amplicon and metagenomic analysis of microbiome data. Protein Cell 12(5):315–330. https://doi.org/10.1007/s13238-020-00724-8

    Article  PubMed  Google Scholar 

  4. Golob JL (2023) Human microbiomes and disease for the biomedical data scientist. Annu Rev Biomed Data Sci. https://doi.org/10.1146/annurev-biodatasci-020722-043017

  5. Athanasopoulou K, Adamopoulos PG, Scorilas A (2023) Unveiling the human gastrointestinal tract microbiome: the past, present, and future of metagenomics. Biomedicine 11(3). https://doi.org/10.3390/biomedicines11030827

  6. Federici S, Nobs SP, Elinav E (2021) Phages and their potential to modulate the microbiome and immunity. Cell Mol Immunol 18(4):889–904. https://doi.org/10.1038/s41423-020-00532-4

    Article  CAS  PubMed  Google Scholar 

  7. d’Herelle M (1961) Sur un microbe invisible antagoniste des bacilles dysentériques. Acta Kravsi

    Google Scholar 

  8. Gregory AC, Zablocki O, Zayed AA, Howell A, Bolduc B, Sullivan MB (2020) The gut Virome database reveals age-dependent patterns of virome diversity in the human gut. Cell Host Microbe 28(5):724–740 e728. https://doi.org/10.1016/j.chom.2020.08.003

  9. Spencer L, Olawuni B, Singh P (2022) Gut Virome: role and distribution in health and gastrointestinal diseases. Front Cell Infect Microbiol 12:836706. https://doi.org/10.3389/fcimb.2022.836706

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Callanan J, Stockdale SR, Shkoporov A, Draper LA, Ross RP, Hill C (2020) Expansion of known ssRNA phage genomes: from tens to over a thousand. Sci Adv 6(6):eaay5981. https://doi.org/10.1126/sciadv.aay5981

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Krishnamurthy SR, Janowski AB, Zhao G, Barouch D, Wang D (2016) Hyperexpansion of RNA bacteriophage diversity. PLoS Biol 14(3):e1002409. https://doi.org/10.1371/journal.pbio.1002409

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Shkoporov AN, Clooney AG, Sutton TDS, Ryan FJ, Daly KM, Nolan JA, McDonnell SA, Khokhlova EV, Draper LA, Forde A, Guerin E, Velayudhan V, Ross RP, Hill C (2019) The human gut virome is highly diverse, stable, and individual specific. Cell Host Microbe 26(4):527–541 e525. https://doi.org/10.1016/j.chom.2019.09.009

  13. Batinovic S, Wassef F, Knowler SA, Rice DTF, Stanton CR, Rose J, Tucci J, Nittami T, Vinh A, Drummond GR, Sobey CG, Chan HT, Seviour RJ, Petrovski S, Franks AE (2019) Bacteriophages in natural and artificial environments. Pathogens 8(3). https://doi.org/10.3390/pathogens8030100

  14. Cao Z, Sugimura N, Burgermeister E, Ebert MP, Zuo T, Lan P (2022) The gut virome: a new microbiome component in health and disease. EBioMedicine 81:104113. https://doi.org/10.1016/j.ebiom.2022.104113

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Hoyles L, McCartney AL, Neve H, Gibson GR, Sanderson JD, Heller KJ, van Sinderen D (2014) Characterization of virus-like particles associated with the human faecal and caecal microbiota. Res Microbiol 165(10):803–812. https://doi.org/10.1016/j.resmic.2014.10.006

    Article  CAS  PubMed  Google Scholar 

  16. Kim MS, Park EJ, Roh SW, Bae JW (2011) Diversity and abundance of single-stranded DNA viruses in human feces. Appl Environ Microbiol 77(22):8062–8070. https://doi.org/10.1128/AEM.06331-11

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Liang G, Bushman FD (2021) The human virome: assembly, composition and host interactions. Nat Rev Microbiol 19(8):514–527. https://doi.org/10.1038/s41579-021-00536-5

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Manrique P, Dills M, Young MJ (2017) The human gut phage community and its implications for health and disease. Viruses 9(6). https://doi.org/10.3390/v9060141

  19. Dutilh BE, Cassman N, McNair K, Sanchez SE, Silva GG, Boling L, Barr JJ, Speth DR, Seguritan V, Aziz RK, Felts B, Dinsdale EA, Mokili JL, Edwards RA (2014) A highly abundant bacteriophage discovered in the unknown sequences of human faecal metagenomes. Nat Commun 5:4498. https://doi.org/10.1038/ncomms5498

    Article  CAS  PubMed  Google Scholar 

  20. Sender R, Fuchs S, Milo R (2016) Revised estimates for the number of human and bacteria cells in the body. PLoS Biol 14(8):e1002533. https://doi.org/10.1371/journal.pbio.1002533

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Zund M, Ruscheweyh HJ, Field CM, Meyer N, Cuenca M, Hoces D, Hardt WD, Sunagawa S (2021) High throughput sequencing provides exact genomic locations of inducible prophages and accurate phage-to-host ratios in gut microbial strains. Microbiome 9(1):77. https://doi.org/10.1186/s40168-021-01033-w

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Guerin E, Hill C (2020) Shining light on human gut bacteriophages. Front Cell Infect Microbiol 10:481. https://doi.org/10.3389/fcimb.2020.00481

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Lourenco M, Chaffringeon L, Lamy-Besnier Q, Pedron T, Campagne P, Eberl C, Berard M, Stecher B, Debarbieux L, De Sordi L (2020) The spatial heterogeneity of the gut limits predation and fosters coexistence of bacteria and bacteriophages. Cell Host Microbe 28(3):390–401 e395. https://doi.org/10.1016/j.chom.2020.06.002

  24. Shkoporov AN, Stockdale SR, Lavelle A, Kondova I, Heuston C, Upadrasta A, Khokhlova EV, van der Kamp I, Ouwerling B, Draper LA, Langermans JAM, Paul Ross R, Hill C (2022) Viral biogeography of the mammalian gut and parenchymal organs. Nat Microbiol 7(8):1301–1311. https://doi.org/10.1038/s41564-022-01178-w

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Cross T, Schoff C, Chudoff D, Graves L, Broomell H, Terry K, Farina J, Correa A, Shade D, Dunbar D (2015) An optimized enrichment technique for the isolation of Arthrobacter bacteriophage species from soil sample isolates. J Vis Exp 98. https://doi.org/10.3791/52781

  26. Carroll-Portillo A, Coffman CN, Varga MG, Alcock J, Singh SB, Lin HC (2021) Standard bacteriophage purification procedures cause loss in numbers and activity. Viruses 13(2). https://doi.org/10.3390/v13020328

  27. Bonilla N, Barr JJ (2018) Phage on tap: a quick and efficient protocol for the preparation of bacteriophage laboratory stocks. Methods Mol Biol 1838:37–46. https://doi.org/10.1007/978-1-4939-8682-8_4

    Article  CAS  PubMed  Google Scholar 

  28. Bonilla N, Rojas MI, Netto Flores Cruz G, Hung SH, Rohwer F, Barr JJ (2016) Phage on tap-a quick and efficient protocol for the preparation of bacteriophage laboratory stocks. PeerJ 4:e2261. https://doi.org/10.7717/peerj.2261

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Xu J, Kiesel B, Kallies R, Jiang FL, Liu Y, Maskow T (2018) A fast and reliable method for monitoring of prophage-activating chemicals. Microb Biotechnol 11(6):1112–1120. https://doi.org/10.1111/1751-7915.13042

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Boling L, Cuevas DA, Grasis JA, Kang HS, Knowles B, Levi K, Maughan H, McNair K, Rojas MI, Sanchez SE, Smurthwaite C, Rohwer F (2020) Dietary prophage inducers and antimicrobials: toward landscaping the human gut microbiome. Gut Microbes 11(4):721–734. https://doi.org/10.1080/19490976.2019.1701353

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Henrot C, Petit MA (2022) Signals triggering prophage induction in the gut microbiota. Mol Microbiol 118(5):494–502. https://doi.org/10.1111/mmi.14983

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Walker PJ, Siddell SG, Lefkowitz EJ, Mushegian AR, Adriaenssens EM, Alfenas-Zerbini P, Davison AJ, Dempsey DM, Dutilh BE, Garcia ML, Harrach B, Harrison RL, Hendrickson RC, Junglen S, Knowles NJ, Krupovic M, Kuhn JH, Lambert AJ, Lobocka M, Nibert ML, Oksanen HM, Orton RJ, Robertson DL, Rubino L, Sabanadzovic S, Simmonds P, Smith DB, Suzuki N, Van Dooerslaer K, Vandamme AM, Varsani A, Zerbini FM (2021) Changes to virus taxonomy and to the International Code of Virus Classification and Nomenclature ratified by the International Committee on Taxonomy of Viruses (2021). Arch Virol 166(9):2633–2648. https://doi.org/10.1007/s00705-021-05156-1

    Article  CAS  PubMed  Google Scholar 

  33. Gallet R, Kannoly S, Wang IN (2011) Effects of bacteriophage traits on plaque formation. BMC Microbiol 11:181. https://doi.org/10.1186/1471-2180-11-181

    Article  PubMed  PubMed Central  Google Scholar 

  34. Marbouty M, Baudry L, Cournac A, Koszul R (2017) Scaffolding bacterial genomes and probing host-virus interactions in gut microbiome by proximity ligation (chromosome capture) assay. Sci Adv 3(2):e1602105. https://doi.org/10.1126/sciadv.1602105

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Modi SR, Lee HH, Spina CS, Collins JJ (2013) Antibiotic treatment expands the resistance reservoir and ecological network of the phage metagenome. Nature 499(7457):219–222. https://doi.org/10.1038/nature12212

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Roux S, Hallam SJ, Woyke T, Sullivan MB (2015) Viral dark matter and virus-host interactions resolved from publicly available microbial genomes. elife 4. https://doi.org/10.7554/eLife.08490

  37. Jovel J, Patterson J, Wang W, Hotte N, O’Keefe S, Mitchel T, Perry T, Kao D, Mason AL, Madsen KL, Wong GK (2016) Characterization of the gut microbiome using 16S or shotgun metagenomics. Front Microbiol 7:459. https://doi.org/10.3389/fmicb.2016.00459

    Article  PubMed  PubMed Central  Google Scholar 

  38. Vernocchi P, Del Chierico F, Putignani L (2016) Gut microbiota profiling: metabolomics based approach to unravel compounds affecting human health. Front Microbiol 7:1144. https://doi.org/10.3389/fmicb.2016.01144

    Article  PubMed  PubMed Central  Google Scholar 

  39. Benler S, Yutin N, Antipov D, Rayko M, Shmakov S, Gussow AB, Pevzner P, Koonin EV (2021) Thousands of previously unknown phages discovered in whole-community human gut metagenomes. Microbiome 9(1):78. https://doi.org/10.1186/s40168-021-01017-w

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Chitcharoen S, Sivapornnukul P, Payungporn S (2022) Revolutionized virome research using systems microbiology approaches. Exp Biol Med (Maywood) 247(13):1135–1147. https://doi.org/10.1177/15353702221102895

    Article  CAS  PubMed  Google Scholar 

  41. Li J, Yang F, Xiao M, Li A (2022) Advances and challenges in cataloging the human gut virome. Cell Host Microbe 30(7):908–916. https://doi.org/10.1016/j.chom.2022.06.003

    Article  CAS  PubMed  Google Scholar 

  42. Khan Mirzaei M, Xue J, Costa R, Ru J, Schulz S, Taranu ZE, Deng L (2021) Challenges of studying the human virome - relevant emerging technologies. Trends Microbiol 29(2):171–181. https://doi.org/10.1016/j.tim.2020.05.021

    Article  CAS  PubMed  Google Scholar 

  43. Hsieh SY, Tariq MA, Telatin A, Ansorge R, Adriaenssens EM, Savva GM, Booth C, Wileman T, Hoyles L, Carding SR (2021) Comparison of PCR versus PCR-free DNA library preparation for characterising the human faecal virome. Viruses 13(10). https://doi.org/10.3390/v13102093

  44. Uritskiy G, Press M, Sun C, Huerta GD, Zayed AA, Wiser A, Grove J, Auch B, Eacker SM, Sullivan S, Bickhart DM, Smith TPL, Sullivan MB, Liachko I (2021) Accurate viral genome reconstruction and host assignment with proximity-ligation sequencing. bioRxiv:2021.2006.2014.448389. https://doi.org/10.1101/2021.06.14.448389

  45. Bowers RM, Clum A, Tice H, Lim J, Singh K, Ciobanu D, Ngan CY, Cheng JF, Tringe SG, Woyke T (2015) Impact of library preparation protocols and template quantity on the metagenomic reconstruction of a mock microbial community. BMC Genomics 16:856. https://doi.org/10.1186/s12864-015-2063-6

    Article  PubMed  PubMed Central  Google Scholar 

  46. Marine R, McCarren C, Vorrasane V, Nasko D, Crowgey E, Polson SW, Wommack KE (2014) Caught in the middle with multiple displacement amplification: the myth of pooling for avoiding multiple displacement amplification bias in a metagenome. Microbiome 2(1):3. https://doi.org/10.1186/2049-2618-2-3

    Article  PubMed  PubMed Central  Google Scholar 

  47. Zuo T, Sun Y, Wan Y, Yeoh YK, Zhang F, Cheung CP, Chen N, Luo J, Wang W, Sung JJY, Chan PKS, Wang K, Chan FKL, Miao Y, Ng SC (2020) Human-gut-DNA virome variations across geography, ethnicity, and urbanization. Cell Host Microbe 28 (5):741–751 e744. https://doi.org/10.1016/j.chom.2020.08.005

  48. Krupovic M, Turner D, Morozova V, Dyall-Smith M, Oksanen HM, Edwards R, Dutilh BE, Lehman SM, Reyes A, Baquero DP, Sullivan MB, Uchiyama J, Nakavuma J, Barylski J, Young MJ, Du S, Alfenas-Zerbini P, Kushkina A, Kropinski AM, Kurtboke I, Brister JR, Lood C, Sarkar BL, Yigang T, Liu Y, Huang L, Wittmann J, Chanishvili N, van Zyl LJ, Rumnieks J, Mochizuki T, Jalasvuori M, Aziz RK, Lobocka M, Stedman KM, Shkoporov AN, Gillis A, Peng X, Enault F, Knezevic P, Lavigne R, Rhee SK, Cvirkaite-Krupovic V, Moraru C, Moreno Switt AI, Poranen MM, Millard A, Prangishvili D, Adriaenssens EM (2021) Bacterial Viruses Subcommittee and Archaeal Viruses Subcommittee of the ICTV: update of taxonomy changes in 2021. Arch Virol 166(11):3239–3244. https://doi.org/10.1007/s00705-021-05205-9

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Creasy A, Rosario K, Leigh BA, Dishaw LJ, Breitbart M (2018) Unprecedented diversity of ssDNA phages from the family microviridae detected within the gut of a protochordate model organism (Ciona robusta). Viruses 10(8). https://doi.org/10.3390/v10080404

  50. Nayfach S, Paez-Espino D, Call L, Low SJ, Sberro H, Ivanova NN, Proal AD, Fischbach MA, Bhatt AS, Hugenholtz P, Kyrpides NC (2021) Metagenomic compendium of 189,680 DNA viruses from the human gut microbiome. Nat Microbiol 6(7):960–970. https://doi.org/10.1038/s41564-021-00928-6

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Szekely AJ, Breitbart M (2016) Single-stranded DNA phages: from early molecular biology tools to recent revolutions in environmental microbiology. FEMS Microbiol Lett 363(6). https://doi.org/10.1093/femsle/fnw027

  52. Manrique P, Bolduc B, Walk ST, van der Oost J, de Vos WM, Young MJ (2016) Healthy human gut phageome. Proc Natl Acad Sci U S A 113(37):10400–10405. https://doi.org/10.1073/pnas.1601060113

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Camarillo-Guerrero LF, Almeida A, Rangel-Pineros G, Finn RD, Lawley TD (2021) Massive expansion of human gut bacteriophage diversity. Cell 184(4):1098–1109. e1099. https://doi.org/10.1016/j.cell.2021.01.029

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Zuppi M, Hendrickson HL, O’Sullivan JM, Vatanen T (2021) Phages in the gut ecosystem. Front Cell Infect Microbiol 11:822562. https://doi.org/10.3389/fcimb.2021.822562

    Article  CAS  PubMed  Google Scholar 

  55. Edwards RA, Vega AA, Norman HM, Ohaeri M, Levi K, Dinsdale EA, Cinek O, Aziz RK, McNair K, Barr JJ, Bibby K, Brouns SJJ, Cazares A, de Jonge PA, Desnues C, Diaz Munoz SL, Fineran PC, Kurilshikov A, Lavigne R, Mazankova K, McCarthy DT, Nobrega FL, Reyes Munoz A, Tapia G, Trefault N, Tyakht AV, Vinuesa P, Wagemans J, Zhernakova A, Aarestrup FM, Ahmadov G, Alassaf A, Anton J, Asangba A, Billings EK, Cantu VA, Carlton JM, Cazares D, Cho GS, Condeff T, Cortes P, Cranfield M, Cuevas DA, De la Iglesia R, Decewicz P, Doane MP, Dominy NJ, Dziewit L, Elwasila BM, Eren AM, Franz C, Fu J, Garcia-Aljaro C, Ghedin E, Gulino KM, Haggerty JM, Head SR, Hendriksen RS, Hill C, Hyoty H, Ilina EN, Irwin MT, Jeffries TC, Jofre J, Junge RE, Kelley ST, Khan Mirzaei M, Kowalewski M, Kumaresan D, Leigh SR, Lipson D, Lisitsyna ES, Llagostera M, Maritz JM, Marr LC, McCann A, Molshanski-Mor S, Monteiro S, Moreira-Grez B, Morris M, Mugisha L, Muniesa M, Neve H, Nguyen NP, Nigro OD, Nilsson AS, O’Connell T, Odeh R, Oliver A, Piuri M, Prussin Ii AJ, Qimron U, Quan ZX, Rainetova P, Ramirez-Rojas A, Raya R, Reasor K, Rice GAO, Rossi A, Santos R, Shimashita J, Stachler EN, Stene LC, Strain R, Stumpf R, Torres PJ, Twaddle A, Ugochi Ibekwe M, Villagra N, Wandro S, White B, Whiteley A, Whiteson KL, Wijmenga C, Zambrano MM, Zschach H, Dutilh BE (2019) Global phylogeography and ancient evolution of the widespread human gut virus crAssphage. Nat Microbiol 4(10):1727–1736. https://doi.org/10.1038/s41564-019-0494-6

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Kirsch JM, Brzozowski RS, Faith D, Round JL, Secor PR, Duerkop BA (2021) Bacteriophage-bacteria interactions in the gut: from invertebrates to mammals. Annu Rev Virol 8(1):95–113. https://doi.org/10.1146/annurev-virology-091919-101238

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Silveira CB, Rohwer FL (2016) Piggyback-the-Winner in host-associated microbial communities. NPJ Biofilms Microbiomes 2:16010. https://doi.org/10.1038/npjbiofilms.2016.10

    Article  PubMed  PubMed Central  Google Scholar 

  58. Kim MS, Bae JW (2018) Lysogeny is prevalent and widely distributed in the murine gut microbiota. ISME J 12(4):1127–1141. https://doi.org/10.1038/s41396-018-0061-9

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. DiGiulio DB, Romero R, Amogan HP, Kusanovic JP, Bik EM, Gotsch F, Kim CJ, Erez O, Edwin S, Relman DA (2008) Microbial prevalence, diversity and abundance in amniotic fluid during preterm labor: a molecular and culture-based investigation. PLoS One 3(8):e3056. https://doi.org/10.1371/journal.pone.0003056

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Breitbart M, Haynes M, Kelley S, Angly F, Edwards RA, Felts B, Mahaffy JM, Mueller J, Nulton J, Rayhawk S, Rodriguez-Brito B, Salamon P, Rohwer F (2008) Viral diversity and dynamics in an infant gut. Res Microbiol 159(5):367–373. https://doi.org/10.1016/j.resmic.2008.04.006

    Article  CAS  PubMed  Google Scholar 

  61. Lim ES, Zhou Y, Zhao G, Bauer IK, Droit L, Ndao IM, Warner BB, Tarr PI, Wang D, Holtz LR (2015) Early life dynamics of the human gut virome and bacterial microbiome in infants. Nat Med 21(10):1228–1234. https://doi.org/10.1038/nm.3950

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Buckley D, Odamaki T, Xiao J, Mahony J, van Sinderen D, Bottacini F (2021) Diversity of human-associated bifidobacterial prophage sequences. Microorganisms 9(12). https://doi.org/10.3390/microorganisms9122559

  63. Huurre A, Kalliomaki M, Rautava S, Rinne M, Salminen S, Isolauri E (2008) Mode of delivery - effects on gut microbiota and humoral immunity. Neonatology 93(4):236–240. https://doi.org/10.1159/000111102

    Article  PubMed  Google Scholar 

  64. Reyes A, Blanton LV, Cao S, Zhao G, Manary M, Trehan I, Smith MI, Wang D, Virgin HW, Rohwer F, Gordon JI (2015) Gut DNA viromes of Malawian twins discordant for severe acute malnutrition. Proc Natl Acad Sci U S A 112(38):11941–11946. https://doi.org/10.1073/pnas.1514285112

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Sharon I, Morowitz MJ, Thomas BC, Costello EK, Relman DA, Banfield JF (2013) Time series community genomics analysis reveals rapid shifts in bacterial species, strains, and phage during infant gut colonization. Genome Res 23(1):111–120. https://doi.org/10.1101/gr.142315.112

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Nagpal R, Shively CA, Appt SA, Register TC, Michalson KT, Vitolins MZ, Yadav H (2018) Gut microbiome composition in non-human primates consuming a Western or Mediterranean diet. Front Nutr 5:28. https://doi.org/10.3389/fnut.2018.00028

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Santoro A, Ostan R, Candela M, Biagi E, Brigidi P, Capri M, Franceschi C (2018) Gut microbiota changes in the extreme decades of human life: a focus on centenarians. Cell Mol Life Sci 75(1):129–148. https://doi.org/10.1007/s00018-017-2674-y

    Article  CAS  PubMed  Google Scholar 

  68. Barr JJ, Auro R, Furlan M, Whiteson KL, Erb ML, Pogliano J, Stotland A, Wolkowicz R, Cutting AS, Doran KS, Salamon P, Youle M, Rohwer F (2013) Bacteriophage adhering to mucus provide a non-host-derived immunity. Proc Natl Acad Sci U S A 110(26):10771–10776. https://doi.org/10.1073/pnas.1305923110

    Article  PubMed  PubMed Central  Google Scholar 

  69. Almeida GMF, Laanto E, Ashrafi R, Sundberg LR (2019) Bacteriophage adherence to mucus mediates preventive protection against pathogenic bacteria. mBio 10(6). https://doi.org/10.1128/mBio.01984-19

  70. Carroll-Portillo A, Lin HC (2021) Exploring mucin as adjunct to phage therapy. Microorganisms 9(3). https://doi.org/10.3390/microorganisms9030509

  71. Looft T, Allen HK, Cantarel BL, Levine UY, Bayles DO, Alt DP, Henrissat B, Stanton TB (2014) Bacteria, phages and pigs: the effects of in-feed antibiotics on the microbiome at different gut locations. ISME J 8(8):1566–1576. https://doi.org/10.1038/ismej.2014.12

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Yan A, Butcher J, Schramm L, Mack DR, Stintzi A (2023) Multiomic spatial analysis reveals a distinct mucosa-associated virome. Gut Microbes 15(1):2177488. https://doi.org/10.1080/19490976.2023.2177488

    Article  PubMed  PubMed Central  Google Scholar 

  73. Furuse K, Osawa S, Kawashiro J, Tanaka R, Ozawa A, Sawamura S, Yanagawa Y, Nagao T, Watanabe I (1983) Bacteriophage distribution in human faeces: continuous survey of healthy subjects and patients with internal and leukaemic diseases. J Gen Virol 64(Pt 9):2039–2043. https://doi.org/10.1099/0022-1317-64-9-2039

    Article  PubMed  Google Scholar 

  74. Lepage P, Colombet J, Marteau P, Sime-Ngando T, Dore J, Leclerc M (2008) Dysbiosis in inflammatory bowel disease: a role for bacteriophages? Gut 57(3):424–425. https://doi.org/10.1136/gut.2007.134668

    Article  CAS  PubMed  Google Scholar 

  75. Kim MS, Bae JW (2016) Spatial disturbances in altered mucosal and luminal gut viromes of diet-induced obese mice. Environ Microbiol 18(5):1498–1510. https://doi.org/10.1111/1462-2920.13182

    Article  CAS  PubMed  Google Scholar 

  76. Ogilvie LA, Jones BV (2015) The human gut virome: a multifaceted majority. Front Microbiol 6:918. https://doi.org/10.3389/fmicb.2015.00918

    Article  PubMed  PubMed Central  Google Scholar 

  77. Marchi J, Zborowsky S, Debarbieux L, Weitz JS (2023) The dynamic interplay of bacteriophage, bacteria and the mammalian host during phage therapy. iScience 26(2):106004. https://doi.org/10.1016/j.isci.2023.106004

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. Mills S, Shanahan F, Stanton C, Hill C, Coffey A, Ross RP (2013) Movers and shakers: influence of bacteriophages in shaping the mammalian gut microbiota. Gut Microbes 4(1):4–16. https://doi.org/10.4161/gmic.22371

    Article  PubMed  PubMed Central  Google Scholar 

  79. Williams HT (2013) Phage-induced diversification improves host evolvability. BMC Evol Biol 13:17. https://doi.org/10.1186/1471-2148-13-17

    Article  PubMed  PubMed Central  Google Scholar 

  80. Brussow H, Canchaya C, Hardt WD (2004) Phages and the evolution of bacterial pathogens: from genomic rearrangements to lysogenic conversion. Microbiol Mol Biol Rev 68 (3):560–602, table of contents. https://doi.org/10.1128/MMBR.68.3.560-602.2004

  81. Hatfull GF (2015) Dark matter of the biosphere: the amazing world of bacteriophage diversity. J Virol 89(16):8107–8110. https://doi.org/10.1128/JVI.01340-15

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. Liu Y, Wang F, Lu H, Fang G, Wen S, Chen C, Shan X, Xu X, Zhang L, Stenzel M, Jin D (2020) Super-resolution mapping of single nanoparticles inside tumor spheroids. Small 16(6):e1905572. https://doi.org/10.1002/smll.201905572

    Article  CAS  PubMed  Google Scholar 

  83. Jung SM, Kim S (2021) In vitro models of the small intestine for studying intestinal diseases. Front Microbiol 12:767038. https://doi.org/10.3389/fmicb.2021.767038

    Article  PubMed  Google Scholar 

  84. Costa J, Ahluwalia A (2019) Advances and current challenges in intestinal in vitro model engineering: a digest. Front Bioeng Biotechnol 7:144. https://doi.org/10.3389/fbioe.2019.00144

    Article  PubMed  PubMed Central  Google Scholar 

  85. Thomas DP, Zhang J, Nguyen NT, Ta HT (2023) Microfluidic gut-on-a-chip: fundamentals and challenges. Biosensors (Basel) 13(1). https://doi.org/10.3390/bios13010136

Download references

Acknowledgments

This work was supported by the Winkler Bacterial Overgrowth Research Fund, BRINM 217.

Author information

Authors and Affiliations

  1. Division of Gastroenterology and Hepatology, University of New Mexico, Albuquerque, NM, USA

    Amanda Carroll-Portillo & Henry C. Lin

  2. Biomedical Research Institute of New Mexico, Albuquerque, NM, USA

    Derek M. Lin

  3. Medicine Service, New Mexico VA Health Care System, Albuquerque, NM, USA

    Henry C. Lin

Authors
  1. Amanda Carroll-Portillo
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Derek M. Lin
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Henry C. Lin
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Amanda Carroll-Portillo .

Editor information

Editors and Affiliations

  1. School of Veterinary Medicine, Texas Tech University, Amarillo, TX, USA

    Ebenezer Tumban

Rights and permissions

Reprints and permissions

Copyright information

© 2024 The Author(s), under exclusive license to Springer Science+Business Media, LLC, part of Springer Nature

About this protocol

Check for updates. Verify currency and authenticity via CrossMark

Cite this protocol

Carroll-Portillo, A., Lin, D.M., Lin, H.C. (2024). The Diversity of Bacteriophages in the Human Gut. In: Tumban, E. (eds) Bacteriophages. Methods in Molecular Biology, vol 2738. Humana, New York, NY. https://doi.org/10.1007/978-1-0716-3549-0_2

Download citation

  • DOI: https://doi.org/10.1007/978-1-0716-3549-0_2

  • Published:

  • Publisher Name: Humana, New York, NY

  • Print ISBN: 978-1-0716-3548-3

  • Online ISBN: 978-1-0716-3549-0

  • eBook Packages: Springer Protocols

Publish with us

Policies and ethics

Search

Navigation