2,035
Views
0
CrossRef citations to date
0
Altmetric
Research Paper

Isolation and characterization of a novel lytic Parabacteroides distasonis bacteriophage φPDS1 from the human gut

ORCID Icon, ORCID Icon, , ORCID Icon, , ORCID Icon, ORCID Icon & ORCID Icon show all
Article: 2298254 | Received 29 Sep 2023, Accepted 19 Dec 2023, Published online: 04 Jan 2024

References

  • Van Belleghem JD, Dąbrowska K, Vaneechoutte M, Barr JJ, Bollyky PL. Interactions between bacteriophage, bacteria, and the mammalian immune system. Viruses. 2018;11(1):10. doi:10.3390/v11010010.
  • Gogokhia L, Buhrke K, Bell R, Hoffman B, Brown DG, Hanke-Gogokhia C, Ajami NJ, Wong MC, Ghazaryan A, Valentine JF, et al. Expansion of bacteriophages is linked to aggravated intestinal inflammation and colitis. Cell Host Microbe. 2019;25:285–299.e8. doi:10.1016/j.chom.2019.01.008.
  • Shkoporov AN, Turkington CJ, Hill C. Mutualistic interplay between bacteriophages and bacteria in the human gut. Nat Rev Microbiol. 2022;20(12):737–24. doi:10.1038/s41579-022-00755-4.
  • Zuo T, Sun Y, Wan Y, Yeoh YK, Zhang F, Cheung CP, Chen N, Luo J, Wang W, Sung JJY, et al. Human-gut-DNA virome variations across geography, ethnicity, and urbanization. Cell Host Microbe. 2020;28(5):741–751.e4. doi:10.1016/j.chom.2020.08.005.
  • Gregory AC, Zablocki O, Zayed AA, Howell A, Bolduc B, Sullivan MB. The gut virome database reveals age-dependent patterns of virome diversity in the human gut. Cell Host Microbe. 2020;28(5):724–740.e8. doi:10.1016/j.chom.2020.08.003.
  • Shareefdeen H, Hill C. The gut virome in health and disease: new insights and associations. Curr Opin Gastroenterol. 2022;38(6):549–554. doi:10.1097/MOG.0000000000000885.
  • Tobin CA, Hill C, Shkoporov AN. Factors affecting variation of the human gut phageome. Annu Rev Microbiol. 2023;77:363–379. doi:10.1146/annurev-micro-032421-105754.
  • Clooney AG, Sutton TDS, Shkoporov AN, Holohan RK, Daly KM, O’Regan O, Ryan FJ, Draper LA, Plevy SE, Ross RP, et al. Whole-virome analysis sheds light on viral dark matter in inflammatory bowel disease. Cell Host Microbe. 2019;26(6):764–778.e5. doi:10.1016/j.chom.2019.10.009.
  • Camarillo-Guerrero LF, Almeida A, Rangel-Pineros G, Finn RD, Lawley TD. Massive expansion of human gut bacteriophage diversity. Cell. 2021;184(4):1098–1109.e9. doi:10.1016/j.cell.2021.01.029.
  • Nayfach S, Páez-Espino D, Call L, Low SJ, Sberro H, Ivanova NN, Proal AD, Fischbach MA, Bhatt AS, Hugenholtz P, et al. Metagenomic compendium of 189,680 DNA viruses from the human gut microbiome. Nat Microbiol. 2021;6(7):960–970. doi: 10.1038/s41564-021-00928-6.
  • Bin Jang H, Bolduc B, Zablocki O, Kuhn JH, Roux S, Adriaenssens EM, Brister JR, Kropinski AM, Krupovic M, Lavigne R, et al. Taxonomic assignment of uncultivated prokaryotic virus genomes is enabled by gene-sharing networks. Nat Biotechnol. 2019;37(6):632–639. doi: 10.1038/s41587-019-0100-8.
  • Turner D, Shkoporov AN, Lood C, Millard AD, Dutilh BE, Alfenas-Zerbini P, van Zyl LJ, Aziz RK, Oksanen HM, Poranen MM, et al. Abolishment of morphology-based taxa and change to binomial species names: 2022 taxonomy update of the ICTV bacterial viruses subcommittee. Arch Virol. 2023;168(2):74. doi: 10.1007/s00705-022-05694-2.
  • Hyman P. Phages for phage therapy: isolation, characterization, and host range breadth. Pharm (Basel). 2019;12(1):35. doi:10.3390/ph12010035.
  • Porter NT, Hryckowian AJ, Merrill BD, Fuentes JJ, Gardner JO, Glowacki RWP, Singh S, Crawford RD, Snitkin ES, Sonnenburg JL, et al. Phase-variable capsular polysaccharides and lipoproteins modify bacteriophage susceptibility in Bacteroides thetaiotaomicron. Nat Microbiol. 2020;5(9):1170–1181. doi: 10.1038/s41564-020-0746-5.
  • Shkoporov AN, Khokhlova EV, Stephens N, Hueston C, Seymour S, Hryckowian AJ, Scholz D, Ross RP, Hill C. Long-term persistence of crAss-like phage crAss001 is associated with phase variation in Bacteroides intestinalis. BMC Biol. 2021;19(1):163. doi:10.1186/s12915-021-01084-3.
  • Wexler AG, Goodman AL. An insider’s perspective: Bacteroides as a window into the microbiome. Nat Microbiol. 2017;2:17026. doi:10.1038/nmicrobiol.2017.26.
  • Cui Y, Zhang L, Wang X, Yi Y, Shan Y, Liu B, Zhou Y, Lü X. Roles of intestinal Parabacteroides in human health and diseases. FEMS Microbiol Lett. 2022;369(1):fnac072. doi:10.1093/femsle/fnac072.
  • Shkoporov AN, Clooney AG, Sutton TDS, Ryan FJ, Daly KM, Nolan JA, McDonnell SA, Khokhlova EV, Draper LA, Forde A, et al. The human gut virome is highly diverse, stable, and individual specific. Cell Host & Microbe. 2019;26(4):527–541.e5. doi:10.1016/j.chom.2019.09.009.
  • Dutilh BE, Cassman N, McNair K, Sanchez SE, Silva GG, Boling L, Barr JJ, Speth DR, Seguritan V, Aziz RK, et al. A highly abundant bacteriophage discovered in the unknown sequences of human faecal metagenomes. Nat Commun. 2014;5:4498. doi:10.1038/ncomms5498.
  • Shkoporov AN, Khokhlova EV, Fitzgerald CB, Stockdale SR, Draper LA, Ross RP, Hill C. ΦCrAss001 represents the most abundant bacteriophage family in the human gut and infects Bacteroides intestinalis. Nat Commun. 2018;9(1):4781. doi:10.1038/s41467-018-07225-7.
  • Smith L, Goldobina E, Govi B, Shkoporov AN. Bacteriophages of the order Crassvirales: what do we currently know about this keystone component of the human gut virome? Biomolecules. 2023;13(4):584. doi:10.3390/biom13040584.
  • Ezeji JC, Sarikonda DK, Hopperton A, Erkkila HL, Cohen DE, Martinez SP, Cominelli F, Kuwahara T, Dichosa AEK, Good CE, et al. Parabacteroides distasonis: intriguing aerotolerant gut anaerobe with emerging antimicrobial resistance and pathogenic and probiotic roles in human health. Gut Microbes. 2021;13(1):1922241. doi:10.1080/19490976.2021.1922241.
  • Guerin E, Shkoporov AN, Stockdale SR, Comas JC, Khokhlova EV, Clooney AG, Daly KM, Draper LA, Stephens N, Scholz D, et al. Isolation and characterisation of ΦcrAss002, a crAss-like phage from the human gut that infects Bacteroides xylanisolvens. Microbiome. 2021;9(1):89. doi:10.1186/s40168-021-01036-7.
  • Luo E, Aylward FO, Mende DR, DeLong EF. Bacteriophage distributions and temporal variability in the ocean’s interior. mBio. 2017;8(6):e01903–e01917. doi:10.1128/mBio.01903-17.
  • Almeida A, Mitchell AL, Boland M, Forster SC, Gloor GB, Tarkowska A, Lawley TD, Finn RD. A new genomic blueprint of the human gut microbiota. Nature. 2019;568(7753):499–504. doi:10.1038/s41586-019-0965-1.
  • Shen J, Zhang J, Mo L, Li Y, Li Y, Li C, Kuang X, Tao Z, Qu Z, Wu L, et al. Large-scale phage cultivation for commensal human gut bacteria. Cell Host Microbe. 2023;31(4):665–677.e7. doi:10.1016/j.chom.2023.03.013.
  • Minot S, Bryson A, Chehoud C, Wu GD, Lewis JD, Bushman FD. Rapid evolution of the human gut virome. Proc Natl Acad Sci U S A. 2013;110(30):12450–51245. doi:10.1073/pnas.1300833110.
  • 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):1228–1234. doi:10.1038/nm.3950.
  • Benler S, Cobián-Güemes AG, McNair K, Hung SH, Levi K, Edwards R, Rohwer F. A diversity-generating retroelement encoded by a globally ubiquitous Bacteroides phage. Microbiome. 2018;6(1):191. doi:10.1186/s40168-018-0573-6.
  • Hedžet S, Rupnik M, Accetto T. Novel Siphoviridae bacteriophages infecting Bacteroides uniformis contain diversity generating retroelement. Microorganisms. 2021;9(5):892. doi:10.3390/microorganisms9050892.
  • Benler S, Yutin N, Antipov D, Rayko M, Shmakov S, Gussow AB, Pevzner P, Koonin EV. Thousands of previously unknown phages discovered in whole-community human gut metagenomes. Microbiome. 2021;9(1):78. doi:10.1186/s40168-021-01017-w.
  • Bean EM, Morella NM, Dey N, Roux S. Complete genome sequences of two Bacteroides uniformis bacteriophages. Microbiol Resour Announc. 2022;11(10):e0061022. doi:10.1128/mra.00610-22.
  • Bakuradze N, Merabishvili M, Kusradze I, Ceyssens PJ, Onsea J, Metsemakers WJ, Grdzelishvili N, Natroshvili G, Tatrishvili T, Lazvliashvili D, et al. Characterization of a bacteriophage GEC_vB_Bfr_UZM3 active against Bacteroides fragilis. Viruses. 2023;15(5):1042. doi:10.3390/v15051042.
  • Quaiser A, Dufresne A, Ballaud F, Roux S, Zivanovic Y, Colombet J, Sime-Ngando T, Francez AJ. Diversity and comparative genomics of Microviridae in Sphagnum- dominated peatlands. Front Microbiol. 2015;6:375. doi:10.3389/fmicb.2015.00375.
  • Creasy A, Rosario K, Leigh BA, Dishaw LJ, Breitbart M. Unprecedented diversity of ssDNA phages from the family Microviridae detected within the gut of a protochordate model organism (Ciona robusta). Viruses. 2018;10(8):404. doi:10.3390/v10080404.
  • Sakamoto M, Benno Y. Reclassification of Bacteroides distasonis, Bacteroides goldsteinii and Bacteroides merdae as Parabacteroides distasonis gen. nov., comb. nov., Parabacteroides goldsteinii comb. nov. and Parabacteroides merdae comb. nov. Int J Syst Evol Microbiol. 2006;56(Pt 7):1599–1605. doi:10.1099/ijs.0.64192-0.
  • Koh GY, Kane A, Lee K, Xu Q, Wu X, Roper J, Mason JB, Crott JW. Parabacteroides distasonis attenuates toll-like receptor 4 signaling and Akt activation and blocks colon tumor formation in high-fat diet-fed azoxymethane-treated mice. Int J Cancer. 2018;143(7):1797–1805. doi:10.1002/ijc.31559.
  • Wang K, Liao M, Zhou N, Bao L, Ma K, Zheng Z, Wang Y, Liu C, Wang W, Wang J, et al. Parabacteroides distasonis alleviates obesity and metabolic dysfunctions via production of succinate and secondary bile acids. Cell Rep. 2019;26(1):222–235.e5. doi:10.1016/j.celrep.2018.12.028.
  • Cuffaro B, Boutillier D, Desramaut J, Jablaoui A, Werkmeister E, Trottein F, Waligora-Dupriet AJ, Rhimi M, Maguin E, Grangette C. Characterization of two Parabacteroides distasonis candidate strains as new live biotherapeutics against obesity. Cells. 2023;12(9):1260. doi:10.3390/cells12091260.
  • Lewis JD, Chen EZ, Baldassano RN, Otley AR, Griffiths AM, Lee D, Bittinger K, Bailey A, Friedman ES, Hoffmann C, et al. Inflammation, antibiotics, and diet as environmental stressors of the gut microbiome in pediatric Crohn’s disease. Cell Host & Microbe. 2015;18(4):489–500. Erratum in: Cell Host Microbe. 2017;22(2):247. doi:10.1016/j.chom.2015.09.008.
  • Cekanaviciute E, Yoo BB, Runia TF, Debelius JW, Singh S, Nelson CA, Kanner R, Bencosme Y, Lee YK, Hauser SL, et al. Gut bacteria from multiple sclerosis patients modulate human T cells and exacerbate symptoms in mouse models. Proc Natl Acad Sci U S A. 2017;114(40):10713–10718. Erratum in: Proc Natl Acad Sci U S A. 2017 Oct 17;114(42):E8943. doi:10.1073/pnas.1711235114.
  • Olbjørn C, Cvancarova Småstuen M, Thiis-Evensen E, Nakstad B, Vatn MH, Jahnsen J, Ricanek P, Vatn S, Moen AEF, Tannæs TM, et al. Fecal microbiota profiles in treatment-naïve pediatric inflammatory bowel disease - associations with disease phenotype, treatment, and outcome. Clin Exp Gastroenterol. 2019;12:37–49. doi:10.2147/CEG.S186235.
  • Sun H, Guo Y, Wang H, Yin A, Hu J, Yuan T, Zhou S, Xu W, Wei P, Yin S, et al. Gut commensal Parabacteroides distasonis alleviates inflammatory arthritis. Gut. 2023;72(9):1664–1677. doi: 10.1136/gutjnl-2022-327756.
  • Wu WKK. Parabacteroides distasonis: an emerging probiotic? Gut. 2023;72(9):1635–1636. doi:10.1136/gutjnl-2022-329386.
  • Dziarski R, Park SY, Kashyap DR, Dowd SE, Gupta D, Mizoguchi E. Pglyrp-regulated gut microflora Prevotella falsenii, Parabacteroides distasonis and Bacteroides eggerthii enhance and Alistipes finegoldii attenuates colitis in mice. PLoS One. 2016;11(1):e0146162. doi:10.1371/journal.pone.0146162.
  • Lopetuso LR, Petito V, Graziani C, Schiavoni E, Paroni Sterbini F, Poscia A, Gaetani E, Franceschi F, Cammarota G, Sanguinetti M, et al. Gut microbiota in health, diverticular disease, irritable bowel syndrome, and inflammatory bowel diseases: time for microbial marker of gastrointestinal disorders. Dig Dis. 2018;36(1):56–65. doi:10.1159/000477205.
  • Yang F, Kumar A, Davenport KW, Kelliher JM, Ezeji JC, Good CE, Jacobs MR, Conger M, West G, Fiocchi C, et al. Complete genome sequence of a Parabacteroides distasonis strain (CavFT hAR46) isolated from a gut wall-cavitating microlesion in a patient with severe Crohn’s disease. Microbiol Resour Announc. 2019;8(36):e00585–19. doi:10.1128/MRA.00585-19.
  • Papenfort K, Bassler BL. Quorum sensing signal-response systems in Gram-negative bacteria. Nat Rev Microbiol. 2016;14(9):576–588. doi:10.1038/nrmicro.2016.89.
  • Hargreaves KR, Kropinski AM, Clokie MR, Kaufmann GF. What does the talking?: Quorum sensing signalling genes discovered in a bacteriophage genome. PLoS One. 2014;9(1):e85131. doi:10.1371/journal.pone.0085131.
  • Silpe JE, Bassler BL. A host-produced quorum-sensing autoinducer controls a phage lysis-lysogeny decision. Cell. 2019;176(1–2):268–280.e13. doi:10.1016/j.cell.2018.10.059.
  • Hendrix H, Zimmermann-Kogadeeva M, Zimmermann M, Sauer U, De Smet J, Muchez L, Lissens M, Staes I, Voet M, Wagemans J, et al. Metabolic reprogramming of Pseudomonas aeruginosa by phage-based quorum sensing modulation. Cell Rep. 2022;38(7):110372. doi:10.1016/j.celrep.2022.110372.
  • Tang F, Bossers A, Harders F, Lu C, Smith H. Comparative genomic analysis of twelve Streptococcus suis (pro)phages. Genomics. 2013;101(6):336–344. doi:10.1016/j.ygeno.2013.04.005.
  • Tarkowski TA, Mooney D, Thomason LC, Stahl FW. Gene products encoded in the ninR region of phage lambda participate in Red-mediated recombination. Genes Cells. 2002;7(4):351–363. doi:10.1046/j.1365-2443.2002.00531.x.
  • De Paepe M, Hutinet G, Son O, Amarir-Bouhram J, Schbath S, Petit MA, Casadesús J. Temperate phages acquire DNA from defective prophages by relaxed homologous recombination: the role of Rad52-like recombinases. PLoS Genet. 2014;10(3):e1004181. doi:10.1371/journal.pgen.1004181.
  • Bryan MJ, Burroughs NJ, Spence EM, Clokie MR, Mann NH, Bryan SJ, Redfield RJ. Evidence for the intense exchange of MazG in marine cyanophages by horizontal gene transfer. PLoS One. 2008;3(4):e2048. doi:10.1371/journal.pone.0002048.
  • Warwick-Dugdale J, Buchholz HH, Allen MJ, Temperton B. Host-hijacking and planktonic piracy: how phages command the microbial high seas. Virol J. 2019;16(1):15. doi:10.1186/s12985-019-1120-1.
  • Hryckowian AJ, Merrill BD, Porter NT, Van Treuren W, Nelson EJ, Garlena RA, Russell DA, Martens EC, Sonnenburg JL. Bacteroides thetaiotaomicron-infecting bacteriophage isolates inform sequence-based host range predictions. Cell Host Microbe. 2020;28(3):371–379.e5. doi:10.1016/j.chom.2020.06.011.
  • Fletcher CM, Coyne MJ, Bentley DL, Villa OF, Comstock LE. Phase-variable expression of a family of glycoproteins imparts a dynamic surface to a symbiont in its human intestinal ecosystem. Proc Natl Acad Sci U S A. 2007;104(7):2413–2418. doi:10.1073/pnas.0608797104.
  • Coyne MJ, Comstock LE. Niche-specific features of the intestinal Bacteroidales. J Bacteriol. 2008;190(2):736–742. doi:10.1128/JB.01559-07.
  • Chamarande J, Cunat L, Alauzet C, Cailliez-Grimal C. In silico study of cell surface structures of Parabacteroides distasonis involved in its maintenance within the gut microbiota. Int J Mol Sci. 2022;23(16):9411. doi:10.3390/ijms23169411.
  • Jiang X, Hall AB, Arthur TD, Plichta DR, Covington CT, Poyet M, Crothers J, Moses PL, Tolonen AC, Vlamakis H, et al. Invertible promoters mediate bacterial phase variation, antibiotic resistance, and host adaptation in the gut. Sci. 2019;363(6423):181–187. doi:10.1126/science.aau5238.
  • Guerin E, Shkoporov A, Stockdale SR, Clooney AG, Ryan FJ, Sutton TDS, Draper LA, González-Tortuero E, Ross RP, Hill C. Biology and taxonomy of crAss-like bacteriophages, the most abundant virus in the human gut. Cell Host Microbe. 2018;24(5):653–664.e6. doi:10.1016/j.chom.2018.10.002.
  • Shkoporov AN, Ryan FJ, Draper LA, Forde A, Stockdale SR, Daly KM, McDonnell SA, Nolan JA, Sutton TDS, Dalmasso M, et al. Reproducible protocols for metagenomic analysis of human faecal phageomes. Microbiome. 2018;6(1):68. doi:10.1186/s40168-018-0446-z.
  • Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics. 2014;30(15):2114–2120. doi:10.1093/bioinformatics/btu170.
  • Callahan BJ, McMurdie PJ, Rosen MJ, Han AW, Johnson AJ, Holmes SP. DADA2: high-resolution sample inference from Illumina amplicon data. Nat Methods. 2016;13(7):581–583. doi:10.1038/nmeth.3869.
  • Edgar RC. UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods. 2013;10(10):996–998. doi:10.1038/nmeth.2604.
  • Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, et al. Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol. 2009;75(23):7537–7541. doi:10.1128/AEM.01541-09.
  • Allard G, Ryan FJ, Jeffery IB, Claesson MJ. SPINGO: a rapid species-classifier for microbial amplicon sequences. BMC Bioinform. 2015;16:324. doi:10.1186/s12859-015-0747-1.
  • Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M, Kulikov AS, Lesin VM, Nikolenko SI, Pham S, Prjibelski AD, et al. Spades: a new genome assembly algorithm and its applications to single-cell sequencing. J Computer Biological. 2012;19(5):455–477. doi:10.1089/cmb.2012.0021.
  • González-Tortuero E, Sutton TDS, Velayudhan V, Shkoporov AN, Draper LA, Stockdale SR, Ross RP, Hill C. VIGA: a sensitive, precise and automatic de novo VIral Genome Annotator. bioRxiv. 2018:277509. doi:10.1101/277509.
  • Zimmermann L, Stephens A, Nam SZ, Rau D, Kübler J, Lozajic M, Gabler F, Söding J, Lupas AN, Alva V. A completely reimplemented MPI bioinformatics toolkit with a new HHpred server at its core. J Mol Biol. 2018;430(15):2237–2243. doi:10.1016/j.jmb.2017.12.007.
  • Grant JR, Enns E, Marinier E, Mandal A, Herman EK, Chen CY, Graham M, Van Domselaar G, Stothard P. Proksee: in-depth characterization and visualization of bacterial genomes. Nucleic Acids Res. 2023;51(W1):W484–W492. doi:10.1093/nar/gkad326.
  • Nayfach S, Camargo AP, Schulz F, Eloe-Fadrosh E, Roux S, Kyrpides NC. CheckV assesses the quality and completeness of metagenome-assembled viral genomes. Nat Biotechnol. 2021;39(5):578–585. doi:10.1038/s41587-020-00774-7.
  • Moraru C, Varsani A, Kropinski AM. VIRIDIC-A novel tool to calculate the intergenomic similarities of prokaryote-infecting viruses. Viruses. 2020;12(11):1268. doi:10.3390/v12111268.
  • Bouras G, Nepal R, Houtak G, Psaltis AJ, Wormald PJ, Vreugde S, Marschall T. Pharokka: a fast scalable bacteriophage annotation tool. Bioinformatics. 2023 Jan 1;39(1):btac776. PMID: 36453861; PMCID: PMC9805569. doi:10.1093/bioinformatics/btac776.
  • Rozewicki J, Li S, Amada KM, Standley DM, Katoh K. MAFFT-DASH: integrated protein sequence and structural alignment. Nucleic Acids Res. 2019;47(W1):W5–W10. doi:10.1093/nar/gkz342.
  • Steenwyk JL, Buida TJ 3rd, Li Y, Shen XX, Rokas A. ClipKIT: a multiple sequence alignment trimming software for accurate phylogenomic inference. PLoS Biol. 2020;18(12):e3001007. doi:10.1371/journal.pbio.3001007.
  • Minh BQ, Schmidt HA, Chernomor O, Schrempf D, Woodhams MD, von Haeseler A, Lanfear R. IQ-TREE 2: new models and efficient methods for phylogenetic inference in the genomic era. Mol Biol Evol. 2020 May 1;37(5):1530–1534. doi:10.1093/molbev/msaa015. Erratum in: Mol Biol Evol. 2020;37(8):2461.
  • Kalyaanamoorthy S, Minh BQ, Wong TKF, von Haeseler A, Jermiin LS. ModelFinder: fast model selection for accurate phylogenetic estimates. Nat Methods. 2017;14(6):587–589. doi:10.1038/nmeth.4285.
  • Menardo F, Loiseau C, Brites D, Coscolla M, Gygli SM, Rutaihwa LK, Trauner A, Beisel C, Borrell S, Gagneux S. Treemmer: a tool to reduce large phylogenetic datasets with minimal loss of diversity. BMC Bioinform. 2018;19(1):164. doi:10.1186/s12859-018-2164-8.
  • Meier-Kolthoff JP, Göker M. VICTOR: genome-based phylogeny and classification of prokaryotic viruses. Bioinformatics. 2017;33(21):3396–3404. doi:10.1093/bioinformatics/btx440.
  • Roux S, Camargo AP, Coutinho FH, Dabdoub SM, Dutilh BE, Nayfach S, Tritt A. iPHoP: an integrated machine learning framework to maximize host prediction for metagenome-derived viruses of archaea and bacteria. PLoS Biol. 2023;21(4):e3002083. doi:10.1371/journal.pbio.3002083.
  • Yu G. Using ggtree to visualize data on tree-like structures. Curr Protoc Bioinformatics. 2020;69(1):e96. doi:10.1002/cpbi.96.
  • Li J, Jia H, Cai X, Zhong H, Feng Q, Sunagawa S, Arumugam M, Kultima JR, Prifti E, Nielsen T, et al. An integrated catalog of reference genes in the human gut microbiome. Nat Biotechnol. 2014;32(8):834–841. doi: 10.1038/nbt.2942.
  • Zhang X, Zhang D, Jia H, Feng Q, Wang D, Liang D, Wu X, Li J, Tang L, Li Y, et al. The oral and gut microbiomes are perturbed in rheumatoid arthritis and partly normalized after treatment. Nat Med. 2015;21(8):895–905. doi: 10.1038/nm.3914.
  • Qin J, Li Y, Cai Z, Li S, Zhu J, Zhang F, Liang S, Zhang W, Guan Y, Shen D, et al. A metagenome-wide association study of gut microbiota in type 2 diabetes. Nature. 2012;490(7418):55–60. doi:10.1038/nature11450.
  • Smits SA, Leach J, Sonnenburg ED, Gonzalez CG, Lichtman JS, Reid G, Knight R, Manjurano A, Changalucha J, Elias JE, et al. Seasonal cycling in the gut microbiome of the Hadza hunter-gatherers of Tanzania. Sci. 2017;357(6353):802–806. doi:10.1126/science.aan4834.
  • Rampelli S, Soverini M, D’Amico F, Barone M, Tavella T, Monti D, Capri M, Astolfi A, Brigidi P, Biagi E, et al. Shotgun metagenomics of gut microbiota in humans with up to extreme longevity and the increasing role of xenobiotic degradation. mSystems. 2020;5(2):e00124–20. doi:10.1128/mSystems.00124-20.
  • Bushnell B. Bbmap: a fast, accurate, Splice-Aware Aligner. Lawrence Berkeley National Laboratory; 2014.
  • Chaumeil PA, Mussig AJ, Hugenholtz P, Parks DH, Borgwardt K. GTDB-Tk v2: memory friendly classification with the genome taxonomy database. Bioinformatics. 2022;38(23):5315–5316. doi:10.1093/bioinformatics/btac672.
  • Antipov D, Korobeynikov A, McLean JS, Pevzner PA. hybridSpades: an algorithm for hybrid assembly of short and long reads. Bioinformatics. 2016;32(7):1009–1015. doi:10.1093/bioinformatics/btv688.