Multiomic spatial analysis reveals a distinct mucosa-associated virome

References

• Tisza MJ, Buck CB. A catalog of tens of thousands of viruses from human metagenomes reveals hidden associations with chronic diseases. Proc Natl Acad Sci. 2021;118(23):e2023202118. doi:10.1073/pnas.2023202118.
   PubMed Web of Science ®Google Scholar
• Liang G, Bushman FD. The human virome: assembly, composition and host interactions. Nat Rev Microbiol. 2021;19(8):514–23. doi:10.1038/s41579-021-00536-5.
   PubMed Web of Science ®Google Scholar
• Shkoporov AN, Hill C. Review Bacteriophages of the Human Gut: the “ Known Unknown “ of the Microbiome. Cell Host Microbe. 2019;25(2):195–209. doi:10.1016/j.chom.2019.01.017.
   PubMed Web of Science ®Google Scholar
• 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(1):527–541.e5. doi:10.1016/j.chom.2019.09.009.
   PubMedGoogle Scholar
• Liang G, Zhao C, Zhang H, Mattei L, Sherrill-Mix S, Bittinger K, Kessler LR, Wu GD, Baldassano RN, DeRusso P, et al. The stepwise assembly of the neonatal virome is modulated by breastfeeding. Nature. 2020;581(7809):470–474. doi:10.1038/s41586-020-2192-1.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Guerin E, Shkoporov A, Stockdale SR, Clooney AG, Ryan FJ, Sutton TDS, Draper LA, Gonzalez-Tortuero E, Ross RP, Hill C, et al. Biology and Taxonomy of crAss-like Bacteriophages, the Most Abundant Virus in the Human Gut. Cell Host Microbe. 2018;24(1):653–664.e6. doi:10.1016/j.chom.2018.10.002.
   PubMedGoogle Scholar
• Koonin EV, Yutin N. The crAss-like Phage Group: how Metagenomics Reshaped the Human Virome. Trends Microbiol. 2020;28(5):349–359. doi:10.1016/j.tim.2020.01.010.
   PubMed Web of Science ®Google Scholar
• 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. Nature Microbiol. 2021;6(7):960–970. doi:10.1038/s41564-021-00928-6.
   PubMed Web of Science ®Google Scholar
• Johansen J, Plichta DR, Nissen JN, Jespersen ML, Shah SA, Deng L, Stokholm J, Bisgaard H, Nielsen DS, Sørensen SJ, et al. Genome binning of viral entities from bulk metagenomics data. Nat Commun. 2022;13(1):965. doi:10.1038/s41467-022-28581-5.
   PubMed Web of Science ®Google Scholar
• Yan A, Butcher J, Mack D, Stintzi A. Virome Sequencing of the Human Intestinal Mucosal–Luminal Interface. Front Cell Infect Microbiol. 2020;10:10. doi:10.3389/fcimb.2020.00010.
   PubMed Web of Science ®Google Scholar
• Garmaeva S, Sinha T, Kurilshikov A, Fu J, Wijmenga C, Zhernakova A, Kurilshikov A, Fu J, Wijmenga C, Zhernakova A, et al. Studying the gut virome in the metagenomic era: challenges and perspectives. BMC Biol. 2019;17:17. doi:10.1186/s12915-019-0636-6.
   PubMed Web of Science ®Google Scholar
• Santiago-Rodriguez TM, Naidu M, Abeles SR, Boehm TK, Ly M, Pride DT. Transcriptome analysis of bacteriophage communities in periodontal health and disease. BMC Genomics. 2015;16(1):549. doi:10.1186/s12864-015-1781-0.
   PubMedGoogle Scholar
• Callanan J, Stockdale SR, Shkoporov A, Draper LA, Ross RP, Hill C. Expansion of known ssRNA phage genomes: from tens to over a thousand. Sci Adv. 2020;6(6):eaay5981. doi:10.1126/sciadv.aay5981.
   PubMed Web of Science ®Google Scholar
• Owen SV, Canals R, Wenner N, Hammarlöf DL, Kröger C, Hinton JCD. A window into lysogeny: revealing temperate phage biology with transcriptomics. Microb Genom. 2020;6(2):e000330. doi:10.1099/mgen.0.000330.
   PubMed Web of Science ®Google Scholar
• Leskinen K, Blasdel BG, Lavigne R, Skurnik M. RNA-Sequencing Reveals the Progression of Phage-Host Interactions between φR1-37 and Yersinia enterocolitica. Viruses. 2016;8(4):111. doi:10.3390/v8040111.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Mottawea W, Butcher J, Li J, Abujamel T, Manoogian J, Mack D, Stintzi A. The mucosal–luminal interface: an ideal sample to study the mucosa-associated microbiota and the intestinal microbial biogeography. Pediatr Res. 2019;85(6):895–903. doi:10.1038/s41390-019-0326-7.
   PubMed Web of Science ®Google Scholar
• Shkoporov AN, Stockdale SR, Lavelle A, Kondova I, Heuston C, Upadrasta A, Khokhlova EV, van der Kamp I, Ouwerling B, Draper LA, et al. Viral biogeography of the mammalian gut and parenchymal organs. Nature Microbiol. 2022;7(8):1301–1311. doi:10.1038/s41564-022-01178-w.
   PubMed Web of Science ®Google Scholar
• Silveira CB, Rohwer FL. Piggyback-the-Winner in host-associated microbial communities. npj Biofilms Microbio. 2016;2(1):16010. doi:10.1038/npjbiofilms.2016.10.
   PubMedGoogle Scholar
• Galley JD, Yu Z, Kumar P, Dowd SE, Lyte M, Bailey MT. The structures of the colonic mucosa-associated and luminal microbial communities are distinct and differentially affected by a prolonged murine stressor. Gut Microbes. 2014;5(6):748–760. doi:10.4161/19490976.2014.972241.
   PubMed Web of Science ®Google Scholar
• Duerkop BA, Condit RC. Bacteriophages shift the focus of the mammalian microbiota. PLoS Pathog. 2018;14(10):e1007310. doi:10.1371/journal.ppat.1007310.
   PubMed Web of Science ®Google Scholar
• Zuo T, Lu X-J, Zhang Y, Cheung CP, Lam S, Zhang F, Tang W, Ching JYL, Zhao R, Chan PKS, et al. Gut mucosal virome alterations in ulcerative colitis. Gut. 2019;2019:1–11.
   Google Scholar
• Adiliaghdam F, Amatullah H, Digumarthi S, Saunders TL, Rahman R-U, Wong LP, Sadreyev R, Droit L, Paquette J, Goyette P, et al. Human enteric viruses autonomously shape inflammatory bowel disease phenotype through divergent innate immunomodulation. Sci Immunol. 2022;7(70):eabn6660–eabn. doi:10.1126/sciimmunol.abn6660.
   PubMed Web of Science ®Google Scholar
• Jiang P, Lai S, Wu S, Zhao X-M, Chen W-H. Host DNA contents in fecal metagenomics as a biomarker for intestinal diseases and effective treatment. BMC Genomics. 2020;21(1):348. doi:10.1186/s12864-020-6749-z.
   PubMed Web of Science ®Google Scholar
• Schroeder KW, Tremaine WJ, Ilstrup DM. Coated Oral 5-Aminosalicylic Acid Therapy for Mildly to Moderately Active Ulcerative Colitis. NEJM. 1987;317(26):1625–1629. doi:10.1056/NEJM198712243172603.
   PubMed Web of Science ®Google Scholar
• Vancuren SJ, Hill JE. Update on cpnDB: a reference database of chaperonin sequences. Database. 2019;2019. doi:10.1093/database/baz033.
   PubMedGoogle Scholar
• Shkoporov AN, Ryan FJ, Draper LA, Forde A, Stockdale SR, Daly KM, Whiteley AS, Murrell JC. Reproducible protocols for metagenomic analysis of human faecal phageomes. Microbiome. 2018;6(1):1–17. doi:10.1186/s40168-017-0383-2.
   PubMedGoogle Scholar
• feargalr. Demovir: taxonomic classification of viruses at Order and Family level; 2019.
   Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• 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. 2013;110(50):20236–20241. doi:10.1073/pnas.1319470110.
   PubMed Web of Science ®Google Scholar
• Lau MCY, Harris RL, Oh Y, Yi MJ, Behmard A, Onstott TC. Taxonomic and Functional Compositions Impacted by the Quality of Metatranscriptomic Assemblies. Front Microbiol. 2018;9. doi:10.3389/fmicb.2018.01235.
   Web of Science ®Google Scholar
• 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):764–78 e5. doi:10.1016/j.chom.2019.10.009.
   PubMed Web of Science ®Google Scholar
• Kim K-H, Bae J-W. Amplification methods bias metagenomic libraries of uncultured single-stranded and double-stranded DNA viruses. Appl Environ Microbiol. 2011;77(21):7663–7668. doi:10.1128/AEM.00289-11.
   PubMed Web of Science ®Google Scholar
• Parras-Moltó M, Rodríguez-Galet A, Suárez-Rodríguez P, López-Bueno A. Evaluation of bias induced by viral enrichment and random amplification protocols in metagenomic surveys of saliva DNA viruses. Microbiome. 2018;6(1):119. doi:10.1186/s40168-018-0507-3.
   PubMedGoogle Scholar
• Vaga S, Lee S, Ji B, Andreasson A, Talley NJ, Agréus L, Bidkhori G, Kovatcheva-Datchary P, Park J, Lee D, et al. Compositional and functional differences of the mucosal microbiota along the intestine of healthy individuals. Sci Rep. 2020;10(1):14977. doi:10.1038/s41598-020-71939-2.
   PubMed Web of Science ®Google Scholar
• Van den Abbeele P, Van de Wiele T, Verstraete W, Possemiers S. The host selects mucosal and luminal associations of coevolved gut microorganisms: a novel concept. FEMS Microbiol Rev. 2011;35(4):681–704. doi:10.1111/j.1574-6976.2011.00270.x.
   PubMed Web of Science ®Google Scholar
• Almeida GMF, Laanto E, Ashrafi R, Sundberg L-R, Martiny JBH. Bacteriophage Adherence to Mucus Mediates Preventive Protection against Pathogenic Bacteria. mBio. 2019;10(6):e01984–19. doi:10.1128/mBio.01984-19.
   PubMed Web of Science ®Google Scholar
• 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. 2013;110(26):10771. doi:10.1073/pnas.1305923110.
   PubMed Web of Science ®Google Scholar
• CUBE UoV. VOGDB: virus Orthologous Groups; 2021.
   Google Scholar
• Grazziotin AL, Koonin EV, Kristensen DM. Prokaryotic Virus Orthologous Groups (pVOGs): a resource for comparative genomics and protein family annotation. Nucleic Acids Res. 2017;45(D1):D491–D8. doi:10.1093/nar/gkw975.
   PubMed Web of Science ®Google Scholar
• Mistry J, Chuguransky S, Williams L, Qureshi M, Salazar Gustavo A, Sonnhammer ELL, Tosatto SCE, Paladin L, Raj S, Richardson LJ, et al. Pfam: the protein families database in 2021. Nucleic Acids Res. 2020;49(D1):D412–D9. doi:10.1093/nar/gkaa913.
   Web of Science ®Google Scholar
• Kanehisa M, Goto S. KEGG: kyoto Encyclopedia of Genes and Genomes. Nucleic Acids Res. 2000;28(1):27–30. doi:10.1093/nar/28.1.27.
   PubMed Web of Science ®Google Scholar
• Haft DH. The TIGRFAMs database of protein families. Nucleic Acids Res. 2003;31(1):371–373. doi:10.1093/nar/gkg128.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Dutilh BE, Cassman N, McNair K, Sanchez SE, Silva GGZ, 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(1). doi:10.1038/ncomms5498.
   PubMedGoogle Scholar
• Gulyaeva A, Garmaeva S, Ruigrok RAAA, Wang D, Riksen NP, Netea MG, Wijmenga C, Weersma RK, Fu J, Vila AV, et al. Discovery, diversity, and functional associations of crAss-like phages in human gut metagenomes from four Dutch cohorts. Cell Rep. 2022;38(2):110204. doi:10.1016/j.celrep.2021.110204.
   PubMed Web of Science ®Google Scholar
• Siranosian BA, Tamburini FB, Sherlock G, Bhatt AS. Acquisition, transmission and strain diversity of human gut-colonizing crAss-like phages. Nat Commun. 2020;11:15.
   PubMed Web of Science ®Google Scholar
• Seemann T. Snippy: rapid haploid variant calling and core genome alignment (version 4.6.0); 2020.
   Google Scholar
• Yutin N, Benler S, Shmakov SA, Wolf YI, Tolstoy I, Rayko M, Antipov D, Pevzner PA, Koonin EV. Analysis of metagenome-assembled viral genomes from the human gut reveals diverse putative CrAss-like phages with unique genomic features. Nat Commun. 2021;12(1):1044. doi:10.1038/s41467-021-21350-w.
   PubMed Web of Science ®Google Scholar
• Yutin N, Makarova KS, Gussow AB, Krupovic M, Segall A, Edwards RA, Koonin EV. Discovery of an expansive bacteriophage family that includes the most abundant viruses from the human gut. Nature Microbiol. 2018;3:38–46. doi:10.1038/s41564-017-0053-y.
   PubMed Web of Science ®Google Scholar
• Minot S, Bryson A. Rapid evolution of the human gut virome. Proc Natl Acad Sci. 2013;110:12450–12455.
   PubMed Web of Science ®Google Scholar
• Roux S, Hallam SJ, Woyke T, Sullivan MB. Viral dark matter and virus–host interactions resolved from publicly available microbial genomes. eLife. 2015;4:e08490. doi:10.7554/eLife.08490.
   PubMed Web of Science ®Google Scholar
• Lourenço M, Chaffringeon L, Lamy-Besnier Q, Pédron T, Campagne P, Eberl C, Bérard M, Stecher B, Debarbieux L, De Sordi L, et al. The Spatial Heterogeneity of the Gut Limits Predation and Fosters Coexistence of Bacteria and Bacteriophages. Cell Host Microbe. 2020;28(1):390–401.e5. doi:10.1016/j.chom.2020.06.002.
   PubMedGoogle Scholar
• Fogg PCM, Rigden DJ, Saunders JR, McCarthy AJ, Allison HE. Characterization of the relationship between integrase, excisionase and antirepressor activities associated with a superinfecting Shiga toxin encoding bacteriophage. Nucleic Acids Res. 2011;39(6):2116–2129. doi:10.1093/nar/gkq923.
   PubMed Web of Science ®Google Scholar
• Balding C, SA B, Pickup RW, Saunders JR. Diversity of phage integrases in Enterobacteriaceae: development of markers for environmental analysis of temperate phages. Environ Microbiol. 2005;7(10):1558–1567. doi:10.1111/j.1462-2920.2005.00845.x.
   PubMed Web of Science ®Google Scholar
• Hannigan GD, Meisel JS, Tyldsley AS, Zheng Q, Hodkinson BP, SanMiguel AJ, Minot S, Bushman FD, and Grice EA. The Human Skin Double-Stranded DNA Virome: topographical and Temporal Diversity, Genetic Enrichment, and Dynamic Associations with the Host Microbiome. mBio. 2015;6(5):e01578–15. doi:10.1128/mBio.01578-15.
   PubMed Web of Science ®Google Scholar
• Hockenberry AJ, Wilke CO. BACPHLIP: predicting bacteriophage lifestyle from conserved protein domains. PeerJ. 2021;9:e11396–e. doi:10.7717/peerj.11396.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Mäntynen S, Laanto E, Oksanen HM, Poranen MM, Díaz-Muñoz SL. Black box of phage-bacterium interactions: exploring alternative phage infection strategies. Open Biol. 2021;11(9):210188. doi:10.1098/rsob.210188.
   PubMed Web of Science ®Google Scholar
• Nami Y, Imeni N, Panahi B. Application of machine learning in bacteriophage research. BMC Microbiol. 2021;21(1):193. doi:10.1186/s12866-021-02256-5.
   PubMed Web of Science ®Google Scholar
• Song K. Classifying the Lifestyle of Metagenomically-Derived Phages Sequences Using Alignment-Free Methods. Front Microbiol. 2020;11. doi:10.3389/fmicb.2020.567769.
   Web of Science ®Google Scholar
• Collier AM, Lyytinen OL, Guo YR, Toh Y, Poranen MM, Tao YJ. Initiation of RNA Polymerization and Polymerase Encapsidation by a Small dsRNA Virus. PLoS Pathog. 2016;12(4):e1005523. doi:10.1371/journal.ppat.1005523.
   PubMed Web of Science ®Google Scholar
• Townsend EM, Kelly L, Muscatt G, Box JD, Hargraves N, Lilley D, Jameson E. The Human Gut Phageome: origins and Roles in the Human Gut Microbiome. Front Cell Infect Microbiol. 2021;11. doi:10.3389/fcimb.2021.643214
   Web of Science ®Google Scholar
• Jimenez-Rivera C, Haas D, Boland M, Barkey JL, Mack DR. Comparison of Two Common Outpatient Preparations for Colonoscopy in Children and Youth. Gastroenterol Res Pract. 2009;2009:518932. doi:10.1155/2009/518932.
   PubMed Web of Science ®Google Scholar
• Mottawea W, Chiang C-K, Mühlbauer M, Starr AE, Butcher J, Abujamel T, Deeke SA, Brandel A, Zhou H, Shokralla S, et al. Altered intestinal microbiota–host mitochondria crosstalk in new onset Crohn’s disease. Nat Commun. 2016;7(1):13419. doi:10.1038/ncomms13419.
   PubMed Web of Science ®Google Scholar
• Stahl M, Friis LM, Nothaft H, Liu X, Li J, Szymanski CM, Stintzi A. l -Fucose utilization provides Campylobacter jejuni with a competitive advantage. Proc Natl Acad Sci. 2011;108(17):7194–7199. doi:10.1073/pnas.1014125108.
   PubMed Web of Science ®Google Scholar
• Schneider VA, Graves-Lindsay T, Howe K, Bouk N, Chen H-C, Kitts PA, Murphy TD, Pruitt KD, Thibaud-Nissen F, Albracht D, et al. Evaluation of GRCh38 and de novo haploid genome assemblies demonstrates the enduring quality of the reference assembly. Genome Res. 2017;27(5):849–864. doi:10.1101/gr.213611.116.
   PubMed Web of Science ®Google Scholar
• Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R. The Sequence Alignment/Map format and SAMtools. bioinformatics. 2009;25(16):2078–2079. doi:10.1093/bioinformatics/btp352.
   PubMed Web of Science ®Google Scholar
• Clarke EL, Taylor LJ, Zhao C, Connell A, Lee J-J, Fett B, Shah P, Lou Y, Ebeling C, Mason AL, et al. Sunbeam: an extensible pipeline for analyzing metagenomic sequencing experiments. Microbiome. 2019;7(1):1–13. doi:10.1186/s40168-018-0604-3.
   PubMedGoogle Scholar
• Kim D, Pertea G, Trapnell C, Pimentel H, Kelley R, Salzberg SL. TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol. 2013;14(4):R36. doi:10.1186/gb-2013-14-4-r36.
   PubMed Web of Science ®Google Scholar
• Kopylova E, Noé L, Touzet H. SortMeRNA: fast and accurate filtering of ribosomal RNAs in metatranscriptomic data. Bioinformatics. 2012;28(24):3211–3217. doi:10.1093/bioinformatics/bts611.
   PubMed Web of Science ®Google Scholar
• Hyatt D, Chen G-L, Locascio PF, Land ML, Larimer FW, Hauser LJ. Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC Bioinform. 2010;11(1):119. doi:10.1186/1471-2105-11-119.
   PubMed Web of Science ®Google Scholar
• Eddy SR. Accelerated Profile HMM Searches. PLoS Comput Biol. 2011;7(10):e1002195. doi:10.1371/journal.pcbi.1002195.
   PubMed Web of Science ®Google Scholar
• Li D, Liu C-M, Luo R, Sadakane K, Lam T-W. MEGAHIT: an ultra-fast single-node solution for large and complex metagenomics assembly via succinct de Bruijn graph. Bioinformatics. 2015;31(10):1674–1676. doi:10.1093/bioinformatics/btv033.
   PubMed Web of Science ®Google Scholar
• Roux S, Bolduc B. Stampede-ClusterGenomes. MAVERICKLab. 2017.https://bitbucket.org/MAVERICLab/stampede-clustergenomes/src/master/
   Google Scholar
• von Meijenfeldt FAB, Arkhipova K, Cambuy DD, Coutinho FH, Dutilh BE. Robust taxonomic classification of uncharted microbial sequences and bins with CAT and BAT. Genome Biol. 2019;20(1):217. doi:10.1186/s13059-019-1817-x.
   PubMed Web of Science ®Google Scholar
• Seemann T. Prokka: rapid prokaryotic genome annotation. Bioinformatics. 2014;30(14):2068–2069. doi:10.1093/bioinformatics/btu153.
   PubMed Web of Science ®Google Scholar
• Steinegger M, Söding J. MMseqs2 enables sensitive protein sequence searching for the analysis of massive data sets. Nat Biotechnol. 2017;35(11):1026–1028. doi:10.1038/nbt.3988.
   PubMed Web of Science ®Google Scholar
• Ziemann M. Accuracy, speed and error tolerance of short DNA sequence aligners. bioRxiv. 2016;053686.
   Google Scholar
• Langmead B, Salzberg SL. Fast gapped-read alignment with Bowtie 2. Nat Methods. 2012;9(4):357–359. doi:10.1038/nmeth.1923.
   PubMed Web of Science ®Google Scholar
• Liao Y, Smyth GK, Shi W. featureCounts: an efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics. 2013;30(7):923–930. doi:10.1093/bioinformatics/btt656.
   PubMed Web of Science ®Google Scholar
• Galiez C, Siebert M, Enault F, Vincent J, Söding J. WIsH: who is the host? Predicting prokaryotic hosts from metagenomic phage contigs. Bioinformatics. 2017;33(19):3113–3114. doi:10.1093/bioinformatics/btx383.
   PubMed Web of Science ®Google Scholar
• McMurdie PJ, Holmes S. phyloseq: an R Package for Reproducible Interactive Analysis and Graphics of Microbiome Census Data. PloS one. 2013;8(4):e61217. doi:10.1371/journal.pone.0061217.
   PubMed Web of Science ®Google Scholar