journal article·2021-02-10Open access

A Novel Singleton Giant Phage Yong-XC31 Lytic to the Pyropia Pathogen Vibrio mediterranei

Lihua Xu, Dengfeng Li, Yigang Tong, Jing Fang, Rui Yang, Weinan Qin, Wei Lin, Lingtin Pan, Wencai Liu

Applied Sciences· Volume 11· Issue 4

Abstract

Vibrio mediterranei 117-T6 is extensively pathogenic to several Pyropia species, leading to the death of conchocelis. In this study, the first V. mediterranei phage (named Vibrio phage Yong-XC31, abbreviated as Yong-XC31) was isolated. Yong-XC31 is a giant phage containing an icosahedral head about 113 nm in diameter and a contractible tail about 219 nm in length. The latent period of Yong-XC31 is 30 min, and burst size is 64,227. Adsorption rate of Yong-XC31 to V. mediterranei 117-T6 can reach 93.8% in 2 min. The phage genome consisted of a linear, double-stranded 290,532 bp DNA molecule with a G + C content of 45.87%. Bioinformatic analyses predicted 318 open reading frames (ORFs), 80 of which had no similarity to protein sequences in current (26 January 2021) public databases. Yong-XC31 shared the highest pair-wise average nucleotide identity (ANI) value of 58.65% (below the ≥95% boundary to define a species) and the highest nucleotide sequence similarity of 11.71% (below the >50% boundary to define a genus) with the closest related phage. In the proteomic tree based on genome-wide sequence similarities, Yong-XC31 and three unclassified giant phages clustered in a monophyletic clade independently between the family Drexlerviridae and Herelleviridae. Results demonstrated Yong-XC31 as a new evolutionary lineage of phage. We propose a new phage family in Caudovirales order. This study provides new insights and fundamental data for the study and application of giant phages.
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Research context

OpenAlex topics: Bacteriophages and microbial interactions · Plant Virus Research Studies · Genomics and Phylogenetic Studies

SciVX discovery tags are terminology-based. OpenAlex topics are source-provided classifications.

Affiliations

Zhejiang Key Laboratory of Marine Biotechnology, Ningbo University, Ningbo 315832, China

Collage of Food and Pharmaceutical Sciences, Ningbo University, Ningbo 315832, China

School of Life Science and Technology, Beijing University of Chemical Technology, Beijing 100029, China

Ocean College, Qinzhou University, Qinzhou 535099, China

References (60)

Show source-provided references
1. Vibrio coralliilyticus sp. nov., a temperature-dependent pathogen of the coral Pocillopora damicornis10.1099/ijs.0.02402-0 ↗
2. Identification of Vibrio harveyi using PCR amplification of the toxR gene10.1111/j.1472-765X.2006.01962.x ↗
3. New Vibrio species associated to molluscan microbiota: A review10.3389/fmicb.2013.00413 ↗
4. A single regulatory gene is sufficient to alter Vibrio aestuarianus pathogenicity in oysters10.1111/1462-2920.12699 ↗
5. New insights into Oculina patagonica coral diseases and their associated Vibrio spp. communities10.1038/ismej.2014.33 ↗
6. Draft genome sequence of a new Vibrio strain with the potential to produce bacteriocin-like inhibitory substances, isolated from the gut microflora of scallop (Argopecten purpuratus)10.1128/genomeA.00419-18 ↗
7. Complete genome sequence of Vibrio mediterranei 117-T6, a potentially pathogenic bacterium isolated from the conchocelis of Pyropia spp.10.1128/MRA.01569-18 ↗
8. Study on yellow spot disease in Pyropia species infected by Vibrio mediterranei 117-T6
9. Economically important red algae resources along the Chinese coast: History, status, and prospects for their utilization10.1016/j.algal.2020.101817 ↗
10. Emerging Vibrio risk at high latitudes in response to ocean warming10.1038/nclimate1628 ↗
11. Climate infuence on Vibrio and associated human diseases during the past half-century in the coastal North Atlantic10.1073/pnas.1609157113 ↗
12. Marine viruses—major players in the global ecosystem10.1038/nrmicro1750 ↗
13. Phage puppet masters of the marine microbial realm10.1038/s41564-018-0166-y ↗
14. Jumbo bacteriophages: An overview10.3389/fmicb.2017.00403 ↗
15. Jumbo bacteriophages
16. Gorski, A., Miedzybrodzki, R., Łobocka, M., Glowackarutkowska, A., Bednarek, A., Borysowski, J., Jonczykmatysiak, E., Łusiakszelachowska, M., Weberdąbrowska, B., and Baginska, N.J.V. (2018). Phage therapy: What have we learned?. Viruses, 10.10.3390/v10060288 ↗
17. Moye, Z.D., Woolston, J., and Sulakvelidze, A. (2018). Bacteriophage applications for food production and processing. Viruses, 10.10.3390/v10040205 ↗
18. Phage-based biocontrol strategies and their application in agriculture and aquaculture10.1042/BST20180178 ↗
19. Bacteriophages: An overview of the control strategies against multiple bacterial infections in different fields10.1002/jobm.201800412 ↗
20. DNA viruses: The really big ones (Giruses)10.1146/annurev.micro.112408.134338 ↗
21. Bacteriophage therapy for the control of Vibrio harveyi in greenlip abalone (Haliotis laevigata)10.1016/j.aquaculture.2017.01.003 ↗
22. Phage preparation FBL1 prevents Bacillus licheniformis biofilm, bacterium responsible for the mortality of the Pacific white shrimp Litopenaeus vannamei10.1016/j.aquaculture.2017.11.007 ↗
23. Protective effects of the Aeromonas phages pAh1-C and pAh6-C against mass mortality of the cyprinid loach (Misgurnus anguillicaudatus) caused by Aeromonas hydrophila10.1016/j.aquaculture.2013.09.045 ↗
24. Characterization and complete genome sequence analysis of a novel virulent Siphoviridae phage against Staphylococcus aureus isolated from bovine mastitis in Xinjiang, China10.1007/s11262-017-1445-z ↗
25. Isolation and characterization of multidrug resistance Aeromonas salmonicida subsp. Salmonicida and its infecting novel phage ASP-1 from goldfish (Carassius auratus)10.1007/s12088-019-00782-5 ↗
26. Adams, M.H. (1959). Bacteriophages, Interscience Publishers Inc.10.5962/bhl.title.6966 ↗
27. Lu, S.G., Le, S., Tan, Y.L., Zhu, J.M., Li, M., Rao, X.C., Zou, L.Y., Li, S., Wang, J., and Jin, X.L. (2013). Genomic and proteomic analyses of the terminally redundant genome of the Pseudomonas aeruginosa phage PaP1: Establishment of genus PaP1-like phages. PLoS ONE, 8.10.1371/journal.pone.0062933 ↗
28. A novel termini analysis theory using HTS data alone for the identification of Enterococcus phage EF4-like genome termini
29. HMMER web server: Interactive sequence similarity searching10.1093/nar/gkr367 ↗
30. The HHpred interactive server for protein homology detection and structure prediction10.1093/nar/gki408 ↗
31. tRNAscan-SE: A program for improved detection of transfer RNA genes in genomic sequence10.1093/nar/25.5.955 ↗
32. NCBI BLAST: A better web interface10.1093/nar/gkn201 ↗
33. OrthoANI: An improved algorithm and software for calculating average nucleotide identity10.1099/ijsem.0.000760 ↗
34. Meier-Kolthoff, J.P., Auch, A.F., Klenk, H.P., and Göker, M. (2013). Genome sequence-based species delimitation with confidence intervals and improved distance functions. BMC Bioinform., 14.10.1186/1471-2105-14-60 ↗
35. A proposed genus boundary for the prokaryotes based on genomic insights10.1128/JB.01688-14 ↗
36. Easyfig: A genome comparison visualizer10.1093/bioinformatics/btr039 ↗
37. Improvements to pairwise sequence comparison (PASC): A genome-based web tool for virus classification10.1007/s00705-014-2197-x ↗
38. ViPTree: The viral proteomic tree server10.1093/bioinformatics/btx157 ↗
39. Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: An international expert proposal for interim standard definitions for acquired resistance10.1111/j.1469-0691.2011.03570.x ↗
40. Mupfunya, C.R., Qekwana, D.N., and Naidoo, V. (2020). Antimicrobial use practices and resistance in indicator bacteria in communal cattle in the Mnisi community, Mpumalanga, South Africa. Vet. Med. Sci.10.1002/vms3.334 ↗
41. Identification and characterization of bacteriophages specific to the catfish pathogen, Edwardsiella ictaluri10.1111/j.1365-2672.2008.03933.x ↗
42. Increased thymidine kinase and thymidylate synthase activities in human epithelial ovarian carcinoma
43. Functional overlap of tRNA nucleotidyltransferase, poly(A) polymerase I, and polynucleotide phosphorylase10.1074/jbc.272.52.33255 ↗
44. Shifting the genomic gold standard for the prokaryotic species definition10.1073/pnas.0906412106 ↗
45. Adriaenssens, E.M., and Brister, J.R. (2017). How to name and classify your phage: An informal guide. Viruses, 9.10.1101/111526 ↗
46. Taxonomy of prokaryotic viruses: 2018-2019 update from the ICTV Bacterial and Archaeal Viruses Subcommittee10.1007/s00705-020-04577-8 ↗
47. Isolation and identification of Vibrio mediterranei 117-T6 as a pathogen associated with yellow spot disease of Pyropia (Bangiales, Rhodophyta)10.1016/j.aquaculture.2020.735372 ↗
48. A review of reported seaweed diseases and pests in aquaculture in Asia10.1111/jwas.12649 ↗
49. Bacteriophage therapy on the conchocelis of Pyropia haitanensis (Rhodophyta) infected by Vibrio mediterranei 117-T610.1016/j.aquaculture.2020.735853 ↗
50. Therapeutic potential of a new jumbo phage that infects Vibrio coralliilyticus, a widespread coral pathogen10.3389/fmicb.2018.02501 ↗
51. The genome of AR9, a giant transducing Bacillus phage encoding two multisubunit RNA polymerases10.1016/j.virol.2016.04.030 ↗
52. Development of giant bacteriophage ϕKZ is independent of the host transcription apparatus10.1128/JVI.01347-14 ↗
53. Extensive proteolysis of head and inner body proteins by a morphogenetic protease in the giant Pseudomonas aeruginosa phage φKZ10.1111/j.1365-2958.2012.08025.x ↗
54. A non-canonical multisubunit RNA polymerase encoded by a giant bacteriophage
55. Cyanophage infection and photoinhibition in marine cyanobacteria10.1016/j.resmic.2004.06.002 ↗
56. Bragg, J.G., and Chisholm, S.W. (2008). Modeling the fitness consequences of a Cyanophage-encoded photosynthesis gene. PLoS ONE, 3.10.1371/journal.pone.0003550 ↗
57. Methyl-accepting chemotaxis proteins: A core sensing element in prokaryotes and archaea10.1007/s00018-017-2514-0 ↗
58. Chemosensory signaling systems that control bacterial survival10.1016/j.tim.2014.04.004 ↗
59. The transcription factor Mlc promotes Vibrio cholerae biofilm formation through repression of phosphotransferase system components10.1128/JB.01639-14 ↗
60. A preliminary X-ray study of a refolded PTS EIIBfruc protein from Escherichia coli10.2174/092986608784967001 ↗