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Unexplored diversity and ecological functions of transposable phages

The ISME Journal volume 17, pages 1015–1028 (2023)Cite this article

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Abstract

Phages are prevalent in diverse environments and play major ecological roles attributed to their tremendous diversity and abundance. Among these viruses, transposable phages (TBPs) are exceptional in terms of their unique lifestyle, especially their replicative transposition. Although several TBPs have been isolated and the life cycle of the representative phage Mu has been extensively studied, the diversity distribution and ecological functions of TBPs on the global scale remain unknown. Here, by mining TBPs from enormous microbial genomes and viromes, we established a TBP genome dataset (TBPGD), that expands the number of accessible TBP genomes 384-fold. TBPs are prevalent in diverse biomes and show great genetic diversity. Based on taxonomic evaluations, we propose the categorization of TBPs into four viral groups, including 11 candidate subfamilies. TBPs infect multiple bacterial phyla, and seem to infect a wider range of hosts than non-TBPs. Diverse auxiliary metabolic genes (AMGs) are identified in the TBP genomes, and genes related to glycoside hydrolases and pyrimidine deoxyribonucleotide biosynthesis are highly enriched. Finally, the influences of TBPs on their hosts are experimentally examined by using the marine bacterium Shewanella psychrophila WP2 and its infecting transposable phage SP2. Collectively, our findings greatly expand the genetic diversity of TBPs, and comprehensively reveal their potential influences in various ecosystems.

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Fig. 1: The distribution of transposable bacteriophages (TBPs) across Earth’s biomes.
Fig. 2: Genome properties of the TBPs.
Fig. 3: Diversity and taxonomic classification of the TBP genome dataset (TBPGD).
Fig. 4: Host distribution of TBPs.
Fig. 5: Distribution of auxiliary metabolic genes (AMGs) encoded by TBPs.
Fig. 6: Influences of the marine transposable phage SP2 on the host transcriptome.

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Data availability

All the identified TBP genomic sequences (n = 18,449) have been deposited in CyVerse (available at https://data.cyverse.org/dav-anon/iplant/home/zhangmujie/TBPGD/TBPGD.zip) and in the National Omics Data Encyclopedia (NODE) under project ID OEP003495. The transcriptomic data from the current study have been deposited in NODE under project ID OEP002984.

References

  1. Dion MB, Oechslin F, Moineau S. Phage diversity, genomics and phylogeny. Nat Rev Microbiol. 2020;18:125–38.

    Article  CAS  PubMed  Google Scholar 

  2. Zimmerman AE, Howard-Varona C, Needham DM, John SG, Worden AZ, Sullivan MB, et al. Metabolic and biogeochemical consequences of viral infection in aquatic ecosystems. Nat Rev Microbiol. 2020;18:21–34.

    Article  CAS  PubMed  Google Scholar 

  3. Feiner R, Argov T, Rabinovich L, Sigal N, Borovok I, Herskovits AA. A new perspective on lysogeny: prophages as active regulatory switches of bacteria. Nat Rev Microbiol. 2015;13:641–50.

    Article  CAS  PubMed  Google Scholar 

  4. Touchon M, Bernheim A, Rocha EP. Genetic and life-history traits associated with the distribution of prophages in bacteria. ISME J. 2016;10:2744–54.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Wahl A, Battesti A, Ansaldi M. Prophages in Salmonella enterica: a driving force in reshaping the genome and physiology of their bacterial host? Mol Microbiol. 2019;111:303–16.

    Article  CAS  PubMed  Google Scholar 

  6. Howard-Varona C, Hargreaves KR, Abedon ST, Sullivan MB. Lysogeny in nature: mechanisms, impact and ecology of temperate phages. ISME J. 2017;11:1511–20.

    Article  PubMed  PubMed Central  Google Scholar 

  7. Argov T, Azulay G, Pasechnek A, Stadnyuk O, Ran-Sapir S, Borovok I, et al. Temperate bacteriophages as regulators of host behavior. Curr Opin Microbiol. 2017;38:81–7.

    Article  CAS  PubMed  Google Scholar 

  8. Toussaint A, Rice PA. Transposable phages, DNA reorganization and transfer. Curr Opin Microbiol. 2017;38:88–94.

    Article  CAS  PubMed  Google Scholar 

  9. Harshey RM. Transposable Phage Mu. Microbiology spectrum. 2014;2. https://doi.org/10.1128/microbiolspec.MDNA3-0007-2014.

  10. Taylor AL. Bacteriophage-induced mutation in Escherichia coli. PNAS 1963;50:1043–51.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Harshey RM. The Mu story: how a maverick phage moved the field forward. Mobile. DNA 2012;3:21.

    CAS  Google Scholar 

  12. Mizuno N, Dramićanin M, Mizuuchi M, Adam J, Wang Y, Han Y-W, et al. MuB is an AAA+ ATPase that forms helical filaments to control target selection for DNA transposition. PNAS 2013;110:E2441–50.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. George M, Bukhari AI. Heterogeneous host DNA attached to the left end of mature bacteriophage Mu DNA. Nature 1981;292:175–6.

    Article  CAS  PubMed  Google Scholar 

  14. Groenen MAM, Putte PVD. Mapping of a site for packaging of bacteriophage Mu DNA. Virology 1985;144:520–2.

    Article  CAS  PubMed  Google Scholar 

  15. Howe MM. Transduction by Bacteriophage MU-l. Virology. 1973;55:103–17.

  16. Gill GS, Hull RC. Mutator bacteriophage D108 and its DNA: an electron microscopic characterization. J Virol. 1981;37:420–30.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Braid MD, Silhavy JL, Kitts CL, Cano RJ, Howe MM. Complete genomic sequence of bacteriophage B3, a Mu-like phage of Pseudomonas aeruginosa. J Bacteriol. 2004;186:6560–74.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Summer EJ, Gonzalez CF, Carlisle T, Mebane LM, Cass AM, Savva CG, et al. Burkholderia cenocepacia phage BcepMu and a family of Mu-like phages encoding potential pathogenesis factors. J Mol Biol. 2004;340:49–65.

    Article  CAS  PubMed  Google Scholar 

  19. Fogg PCM, Hynes AP, Digby E, Lang AS, Beatty JT. Characterization of a newly discovered Mu-like bacteriophage, RcapMu, in Rhodobacter capsulatus strain SB1003. Virology 2011;421:211–21.

    Article  CAS  PubMed  Google Scholar 

  20. Zehr ES, Tabatabai LB, Bayles DO. Genomic and proteomic characterization of SuMu, a Mu-like bacteriophage infecting Haemophilus parasuis. BMC Genom. 2012;13:331.

    Article  CAS  Google Scholar 

  21. Jakhetia R, Verma NK. Identification and Molecular Characterisation of a Novel Mu-Like Bacteriophage, SfMu, of Shigella flexneri. PLoS ONE. 2015;10:e0124053.

    Article  PubMed  PubMed Central  Google Scholar 

  22. Wu H, Zhang Y, Jiang Y, Wu H, Sun W, Huang Y-P. Characterization and Genomic Analysis of ΦSHP3, a New Transposable Bacteriophage Infecting Stenotrophomonas maltophilia. J Virol. 2021;95:e00019–21.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Masignani V, Giuliani MM, Tettelin H, Comanducci M, Rappuoli R, Scarlato V. Mu-like Prophage in serogroup B Neisseria meningitidis coding for surface-exposed antigens. Infect Immun. 2001;69:2580–8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Morgan GJ, Hatfull GF, Casjens S, Hendrix RW. Bacteriophage Mu Genome Sequence Analysis and comparision with Mu-like prophages in Haemophilus, Neisseria and Deinococcus. J Mol Microbiol. 2002;317:337–59.

    CAS  Google Scholar 

  25. Guo Q, Chen B, Tu Y, Du S, Chen X. Prophage LambdaSo uses replication interference to suppress reproduction of coexisting temperate phage MuSo2 in Shewanella oneidensis MR-1. Environ Microbiol. 2019;21:2079–94.

    Article  CAS  PubMed  Google Scholar 

  26. Tang K, Lin D, Zheng Q, Liu K, Yang Y, Han Y, et al. Genomic, proteomic and bioinformatic analysis of two temperate phages in Roseobacter clade bacteria isolated from the deep-sea water. BMC Genom. 2017;18:485.

    Article  Google Scholar 

  27. Szafrański SP, Kilian M, Yang I. Wieden GBd, Winkel A, Hegermann J, et al. Diversity patterns of bacteriophages infecting Aggregatibacter and Haemophilus species across clades and niches. ISME J. 2019;13:2500–22.

    Article  PubMed  PubMed Central  Google Scholar 

  28. Cui Z, Xu Z, Wei Y, Zhang Q, Qin K, Ji X. Characterization and Genome Analysis of a Novel Mu-like Phage VW-6B Isolated from the Napahai Plateau Wetland of China. Curr Microbiol. 2021;78:150–8.

    Article  CAS  PubMed  Google Scholar 

  29. Lin D, Tang K, Han Y, Li C, Chen X. Genome sequence of an inducible phage in Rhodovulum sp. P5 isolated from the shallow-sea hydrothermal system. Mar Genom. 2016;30:93–5.

    Article  Google Scholar 

  30. Mara P, Vik D, Pachiadaki MG, Suter EA, Poulos B, Taylor GT, et al. Viral elements and their potential influence on microbial processes along the permanently stratified Cariaco Basin redoxcline. ISME J. 2020;14:3079–92.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Hulo C, Masson P, Mercier PL, Toussaint A. A structured annotation frame for the transposable phages: a new proposed family “Saltoviridae” within the Caudovirales. Virology 2015;477:155–63.

    Article  CAS  PubMed  Google Scholar 

  32. Toussaint A, Gijsegem FV. Extension of the transposable bacterial virus family: two genomic organisations among phages and prophages with a Tn552-related transposase. Res Microbiol. 2018;169:495–9.

    Article  CAS  PubMed  Google Scholar 

  33. Ndela EO, Enault F, Toussaint A. Transposable Prophages in Leptospira: An Ancient, Now Diverse, Group Predominant in Causative Agents of Weil’s Disease. Int J Mol Sci. 2021;22:13434.

    Article  Google Scholar 

  34. Aziz RK, Breitbart M, Edwards RA. Transposases are the most abundant, most ubiquitous genes in nature. Nucleic Acids Res. 2010;38:4207–17.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Paez-Espino D, Roux S, Chen I-MA, Palaniappan K, Ratner A, Chu K, et al. IMG/VR v.2.0: an integrated data management and analysis system for cultivated and environmental viral genomes. Nucleic Acids Res. 2019;47:D678–D86.

    Article  CAS  PubMed  Google Scholar 

  36. Gregory AC, Zayed AA, Conceição-Neto N, Temperton B, Bolduc B, Alberti A, et al. Marine DNA Viral Macro- and Microdiversity from Pole to Pole. Cell 2019;177:1109–23.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Turner D, Kropinski AM, Adriaenssens EM. A Roadmap for Genome-Based Phage Taxonomy. Viruses 2021;13:506.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Parks DH, Chuvochina M, Rinke C, Mussig AJ, Chaumeil P-A, Hugenholtz P. GTDB: an ongoing census of bacterial and archaeal diversity through a phylogenetically consistent, rank normalized and complete genome-based taxonomy. Nucleic Acids Res. 2022;50:D785–D94.

    Article  CAS  PubMed  Google Scholar 

  39. Ritacco CJ, Kamtekar S, Wang J, Steitz TA. Crystal structure of an intermediate of rotating dimers within the synaptic tetramer of the G-segment invertase. Nucleic Acids Res. 2013;41:2673–82.

    Article  CAS  PubMed  Google Scholar 

  40. Howe MM, Pato ML. Phage Mu. Reference Module in Life Sciences. 2017:1–6. https://doi.org/10.1016/B978-0-12-809633-8.06883-7.

  41. Shaffer M, Borton MA, McGivern BB, Zayed AA, Rosa SLL, Solden LM, et al. DRAM for distilling microbial metabolism to automate the curation of microbiome function. Nucleic Acids Res. 2020;48:8883–900.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Xiao X, Wang P, Zeng X, Bartlett DH, Wang F. Shewanella psychrophila sp. nov. and Shewanella piezotolerans sp. nov., isolated from west Pacific deep-sea sediment. Int J Syst Evolut Microbiol. 2007;57:60–5.

    Article  CAS  Google Scholar 

  43. Xu G, Jian H, Xiao X, Wang F. Complete genome sequence of Shewanella psychrophila WP2, a deep-sea bacterium isolated from west Pacific sediment. Mar Genom. 2017;35:19–21.

    Article  Google Scholar 

  44. Namgoong S-Y, M.Harshey R. The same two monomers within a MuA tetramer provide the DDE domains for the strand cleavage and strand transfer steps of transposition. EMBO J. 1988;17:3775–85.

    Article  Google Scholar 

  45. Mizuuchi M, Mizuuchi K. Conformational isomerization in phage Mu transpososome assembly effects of the transpositional enhancer and of MuB. EMBO J. 2001;20:6927–35.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Han Y-W, Mizuuchi K. Phage Mu transposition immunity: protein pattern formation along DNA by a diffusion-ratchet mechanism. Mol Cell. 2010;39:48–58.

    Article  PubMed  PubMed Central  Google Scholar 

  47. Choi W, Jang S, Harshey RM. Mu transpososome and RecBCD nuclease collaborate in the repair of simple Mu insertions. PNAS 2014;111:14112–7.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Wang PW, Chu L, Guttman DS. Complete sequence and evolutionary genomic analysis of the Pseudomonas aeruginosa transposable bacteriophage D3112. J Bacteriol. 2004;186:400–10.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Goudie AD, Lynch KH, Seed KD, Stothard P, Shrivastava S, Wishart DS, et al. Genomic sequence and activity of KS10, a transposable phage of the Burkholderia cepacia complex. BMC Genom. 2008;9:615.

    Article  Google Scholar 

  50. Chung I-Y, Cho Y-H. Complete genome sequences of two Pseudomonas aeruginosa temperate phages, MP29 and MP42, which lack the phage-host CRISPR interaction. J Virol. 2012;86:8336.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Yang J, Kong Y, Li X, Yang S. A novel transposable Mu-like prophage in Bacillus alcalophilus CGMCC 1.3604 (ATCC 27647). Virol Sin. 2015;30:63–5.

    Article  PubMed  PubMed Central  Google Scholar 

  52. Thi BVT, Khanh NHP, Namikawa R, Miki K, Kondo A, Thi PTD, et al. Genomic characterization of Ralstonia solanacearum phage ΦRS138 of the family Siphoviridae. Arch Virol. 2016;161:483–6.

    Article  Google Scholar 

  53. Cornuault JK, Petit M-A, Mariadassou M, Benevides L, Moncaut E, Langella P, et al. Phages infecting Faecalibacterium prausnitzii belong to novel viral genera that help to decipher intestinal viromes. Microbiome 2018;6:65.

    Article  PubMed  PubMed Central  Google Scholar 

  54. Toussaint A. Transposable Mu-like phages in Firmicutes: new instances of divergence generating retroelements. Res Microbiol. 2013;164:281–7.

    Article  CAS  PubMed  Google Scholar 

  55. Cazares A, Mendoza-Hernández G, Guarneros G. Core and accessory genome architecture in a group of Pseudomonas aeruginosa Mu-like phages. BMC Genom. 2014;15:1146.

  56. Touchon M, Sousa JAMD, Rocha EP. Embracing the enemy: the diversification of microbial gene repertoires by phage-mediated horizontal gene transfer. Curr Opin Microbiol. 2017;38:66–73.

    Article  CAS  PubMed  Google Scholar 

  57. Edlin G, Lin L, Bitner R. Reproductive fitness of P1, P2, and Mu lysogens of Escherichia coli. J Virol. 1977;21:560–4.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Engelhardt T, Sahlberg M, Cypionka H, Engelen B. Biogeography of Rhizobium radiobacter and distribution of associated temperate phages in deep subseafloor sediments. ISME J. 2013;7:199–209.

    Article  CAS  PubMed  Google Scholar 

  59. Fredrickson JK, Romine MF, Beliaev AS, Auchtung JM, Driscoll ME, Gardner TS, et al. Towards environmental systems biology of Shewanella. Nat Rev Microbiol. 2008;6:592–603.

    Article  CAS  PubMed  Google Scholar 

  60. Lemaire ON, Méjean V, Iobbi-Nivol C. The Shewanella genus: ubiquitous organisms sustaining and preserving aquatic ecosystems. FEMS Microbiol Rev. 2020;44:155–70.

    Article  CAS  PubMed  Google Scholar 

  61. Hickman AB, Dyda F. DNA Transposition at Work. Chem Rev. 2016;116:12758–84.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Roux S, Krupovic M, Daly RA, Borges AL, Nayfach S, Schulz F, et al. Cryptic inoviruses revealed as pervasive in bacteria and archaea across Earth’s biomes. Nat Microbiol. 2019;4:1895–906.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Sayers EW, Cavanaugh M, Clark K, Pruitt KD, Schoch CL, Sherry ST, et al. GenBank. Nucleic Acids Res. 2021;49:D92–D6.

    Article  CAS  PubMed  Google Scholar 

  64. Lefkowitz EJ, Dempsey DM, Hendrickson RC, Orton RJ, Siddell SG, Smith DB. Virus taxonomy: the database of the International Committee on Taxonomy of Viruses (ICTV). Nucleic Acids Res. 2018;46:D708–D17.

    Article  CAS  PubMed  Google Scholar 

  65. Steinegger M, Meier M, Mirdita M, Vöhringer H, Haunsberger SJ, Söding J. HH-suite3 for fast remote homology detection and deep protein annotation. BMC Bioinform. 2019;20:473.

    Article  Google Scholar 

  66. Mistry J, Chuguransky S, Williams L, Qureshi M, Salazar GA, Sonnhammer ELL, et al. Pfam: The protein families database in 2021. Nucleic Acids Res. 2021;49:D412–D9.

    Article  CAS  PubMed  Google Scholar 

  67. Muhire BM, Varsani A, Martin DP. SDT: a virus classification tool based on pairwise sequence alignment and identity calculation. PLoS ONE. 2014;9:e108277.

    Article  PubMed  PubMed Central  Google Scholar 

  68. Jumper J, Evans R, Pritzel A, Green T, Figurnov M, Ronneberger O, et al. Highly accurate protein structure prediction with AlphaFold. Nature 2021;596:583–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Holm L. Using Dali for Protein Structure Comparison. In: Gάspάri Z, editor. Structural Bioinformatics: Methods and Protocols. Methods in Molecular Biology. Springer Science+Business Media; 2020;2112:29–42.

  70. Li W, O’Neill KR, Haft DH, DiCuccio M, Chetvernin V, Badretdin A, et al. RefSeq: expanding the Prokaryotic Genome Annotation Pipeline reach with protein family model curation. Nucleic Acids Res. 2021;49:D1020–D8.

    Article  CAS  PubMed  Google Scholar 

  71. O’Leary NA, Wright MW, Brister JR, Ciufo S, Haddad D, McVeigh R, et al. Reference sequence (RefSeq) database at NCBI: current status, taxonomic expansion, and functional annotation. Nucleic Acids Res. 2016;44:D733–45.

    Article  PubMed  Google Scholar 

  72. Grigoriev IV, Nordberg H, Shabalov I, Aerts A, Cantor M, Goodstein D, et al. The genome portal of the Department of Energy Joint Genome Institute. Nucleic Acids Res. 2012;40:D26–32.

    Article  CAS  PubMed  Google Scholar 

  73. Nordberg H, Cantor M, Dusheyko S, Hua S, Poliakov A, Shabalov I, et al. The genome portal of the Department of Energy Joint Genome Institute: 2014 updates. Nucleic Acids Res. 2014;42:D26–31.

    Article  CAS  PubMed  Google Scholar 

  74. Bolduc B, Zablocki O, Guo J, Zayed AA, Vik D, Dehal P, et al. iVirus 2.0: Cyberinfrastructure-supported tools and data to power DNA virus ecology. ISME Commun. 2021;1:77.

    Article  PubMed  PubMed Central  Google Scholar 

  75. 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;11:119.

    Article  Google Scholar 

  76. Potter SC, Luciani A, Eddy SR, Park Y, Lopez R, Finn RD. HMMER web server: 2018 update. Nucleic Acids Res. 2018;46:W200–W4.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J, Bealer K, et al. BLAST+: architecture and applications. BMC Bioinform. 2009;10:421.

    Article  Google Scholar 

  78. Buchfink B, Xie C, Huson DH. Fast and sensitive protein alignment using DIAMOND. Nat Methods. 2015;12:59–60.

    Article  CAS  PubMed  Google Scholar 

  79. Terzian P, Ndela EO, Galiez C, Lossouarn J, Bucio REP, Mom R, et al. PHROG: families of prokaryotic virus proteins clustered using remote homology. NAR Genom Bioinforma. 2021;3:lqab067.

    Article  Google Scholar 

  80. Fu L, Niu B, Zhu Z, Wu S, Li W. CD-HIT: accelerated for clustering the next-generation sequencing data. Bioinformatics 2012;28:3150–2.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  81. Roux S, Adriaenssens EM, Dutilh BE, Koonin EV, Kropinski AM, Krupovic M, et al. Minimum Information about an Uncultivated Virus Genome (MIUViG). Nat Biotechnol. 2019;37:29–37.

    Article  CAS  PubMed  Google Scholar 

  82. Jang HB, Bolduc B, Zablocki O, Kuhn JH, Roux S, Adriaenssens EM, et al. Taxonomic assignment of uncultivated prokaryotic virus genomes is enabled by gene-sharing networks. Nat Biotechnol. 2019;37:632–9.

    Article  Google Scholar 

  83. Shannon P, Andrew M, Ozier O, Baliga NS, Wang JT, Ramage D, et al. Cytoscape A Software Environment for Integrated Models of Biomolecular Interaction Networks. Genome Res. 2003;13:2498–504.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. Jiang J-Z, Yuan W-G, Shang J, Shi Y-H, Yang L-L, Liu M, et al. Virus classification for viral genomic fragments using PhaGCN2. Brief Bioinforma. 2023;24:1–9.

    Article  Google Scholar 

  85. Chaumeil P-A, Mussig AJ, Hugenholtz P, Parks DH. GTDB-Tk: a toolkit to classify genomes with the Genome Taxonomy Database. Bioinformatics 2020;36:1925–7.

    Article  CAS  Google Scholar 

  86. Matsen FA, Kodner RB, Armbrust EV. pplacer: linear time maximum-likelihood and bayesian phylogenetic placement of sequences onto a fixed reference tree. BMC Bioinform. 2010;11:538.

    Article  Google Scholar 

  87. Consortium TU. UniProt: the universal protein knowledgebase in 2021. Nucleic Acids Res. 2021;49:D480–D9.

    Article  Google Scholar 

  88. Yan F, Yu X, Duan Z, Lu J, Jia B, Qiao Y, et al. Discovery and characterization of the evolution, variation and functions of diversity-generating retroelements using thousands of genomes and metagenomes. BMC Genom. 2019;20:595.

    Article  Google Scholar 

  89. Jian H, Yi Y, Wang J, Hao Y, Zhang M, Wang S, et al. Diversity and distribution of viruses inhabiting the deepest ocean on Earth. ISME J. 2021;15:3094–110.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  90. Bland C, Ramsey TL, Sabree F, Lowe M, Brown K, Kyrpides NC, et al. CRISPR recognition tool (CRT): a tool for automatic detection of clustered regularly interspaced palindromic repeats. BMC Bioinform. 2007;8:209.

    Article  Google Scholar 

  91. Paez-Espino D, Eloe-Fadrosh EA, Pavlopoulos GA, Thomas AD, Huntemann M, Mikhailova N, et al. Uncovering Earth’s virome. Nature 2016;536:425–30.

    Article  CAS  PubMed  Google Scholar 

  92. Guo J, Bolduc B, Zayed AA, Varsani A, Dominguez-Huerta G, Delmont TO, et al. VirSorter2: a multi-classifier, expert-guided approach to detect diverse DNA and RNA viruses. Microbiome 2021;9:37.

    Article  PubMed  PubMed Central  Google Scholar 

  93. Kanehisa M, Furumichi M, Sato Y, Ishiguro-Watanabe M, Tanabe M. KEGG: integrating viruses and cellular organisms. Nucleic Acids Res. 2021;49:D545–D51.

    Article  CAS  PubMed  Google Scholar 

  94. Chan PP, Lin BY, Mak AJ, Lowe TM. tRNAscan-SE 2.0: improved detection and functional classification of transfer RNA genes. Nucleic Acids Res. 2021;49:9077–96.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  95. Ahlmann-Eltze C, Patil I. Ggsignif: R package for displaying significance brackets for ‘ggplot2’. PsyArXiv. 2021. https://doi.org/10.31234/osf.io/7awm6.

  96. Virtanen P, Gommers R, Oliphant TE, Haberland M, Reddy T, Cournapeau D, et al. SciPy 1.0: fundamental algorithms for scientific computing in Python. Nat Methods. 2020;17:261–72.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  97. Robinson MD, McCarthy DJ, Smyth GK. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 2010;26:139–40.

    Article  CAS  PubMed  Google Scholar 

  98. Benjamini Y, Hochberg Y. Controlling the False Discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc: Ser B (Methodol). 1995;1:289–300.

    Google Scholar 

  99. Meng C, Li S, Fan Q, Chen R, Hu Y, Xiao X, et al. The thermo-regulated genetic switch of deep-sea filamentous phage SW1 and its distribution in the Pacific Ocean. FEMS Microbiol Lett. 2020;367:fnaa094.

    Article  CAS  PubMed  Google Scholar 

  100. Hurwitz BL, Sullivan MB. The Pacific Ocean virome (POV): a marine viral metagenomic dataset and associated protein clusters for quantitative viral ecology. PLoS ONE. 2013;8:e57355.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  101. Jian H, Xiao X, Wang F. Role of filamentous phage SW1 in regulating the lateral flagella of Shewanella piezotolerans strain WP3 at low temperatures. Appl Environ Microbiol. 2013;79:7101–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  102. Ye J, Coulouris G, Zaretskaya I, Cutcutache I, Rozen S, Madden TL. Primer-BLAST: A tool to design target-specific primers for polymerase chain reaction. BMC Bioinform. 2012;13:134.

    Article  CAS  Google Scholar 

  103. Jian H, Xu G, Yi Y, Hao Y, Wang Y, Xiong L, et al. The origin and impeded dissemination of the DNA phosphorothioation system in prokaryotes. Nat Commun. 2021;12:6382.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  104. Chen S, Zhou Y, Chen Y, Gu J. fastp: an ultra-fast all-in-one FASTQ preprocessor. Bioinformatics 2018;34:i884–i90.

    Article  PubMed  PubMed Central  Google Scholar 

  105. Kim D, Langmead B, Salzberg SL. HISAT: a fast spliced aligner with low memory requirements. Nat Methods. 2015;12:357–60.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  106. Li B, Dewey CN. RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinform. 2011;12:323.

    Article  CAS  Google Scholar 

  107. Wang L, Feng Z, Wang X, Wang X, Zhang X. DEGseq: an R package for identifying differentially expressed genes from RNA-seq data. Bioinformatics 2010;26:136–8.

    Article  PubMed  Google Scholar 

  108. Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, Baren MJV, et al. Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol. 2010;28:511–5.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

This work was financially supported by the Hainan Provincial Joint Project of Sanya Yazhou Bay Science and Technology City (grant no. 2021JJLH0057), the National Natural Science Foundation of China (grant nos. 42176095, 91851113, 41921006), the National Key R&D Program of China (grant no. 2021YFF0501300), and the Oceanic Interdisciplinary Program of Shanghai Jiao Tong University (project no. SL2021PT201). We would like to thank Prof. Ariane Toussaint for helpful suggestions on TBP identification. We are grateful to the editor and two anonymous reviewers for their comments that were instrumental in improving the paper.

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Authors and Affiliations

  1. State Key Laboratory of Microbial Metabolism, Joint International Research Laboratory of Metabolic & Development Sciences, School of Life Sciences and Biotechnology, Shanghai Jiao Tong University, Shanghai, China

    Mujie Zhang, Yali Hao, Yi Yi, Shunzhang Liu, Qingyang Sun, Xiaoli Tan, Shan Tang, Xiang Xiao & Huahua Jian

  2. Southern Marine Science and Engineering Guangdong Laboratory (Zhuhai), Zhuhai, China

    Xiang Xiao

  3. Yazhou Bay Institute of Deepsea Sci-Tech, Shanghai Jiao Tong University, Sanya, China

    Xiang Xiao & Huahua Jian

Authors
  1. Mujie Zhang
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  2. Yali Hao
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  3. Yi Yi
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  4. Shunzhang Liu
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  5. Qingyang Sun
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  6. Xiaoli Tan
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  7. Shan Tang
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  8. Xiang Xiao
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  9. Huahua Jian
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Contributions

HJ conceived and designed the research; MZ, QS, and ST collected and curated genomic and metadata; MZ performed the bioinformatic and statistical analysis; MZ and SL conducted the microbiological experiments; YH and XT helped in RNA isolation; MZ and HJ analyzed and interpreted the data; HJ and MZ wrote the paper; XX and YY provided useful comments to improve the paper; HJ supervised the project. All the authors reviewed the results and approved the paper.

Corresponding author

Correspondence to Huahua Jian.

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Zhang, M., Hao, Y., Yi, Y. et al. Unexplored diversity and ecological functions of transposable phages. ISME J 17, 1015–1028 (2023). https://doi.org/10.1038/s41396-023-01414-z

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  • DOI: https://doi.org/10.1038/s41396-023-01414-z

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