Bacillus subtilis phage phi18: genomic analysis and receptor identification.


Journal

Archives of virology
ISSN: 1432-8798
Titre abrégé: Arch Virol
Pays: Austria
ID NLM: 7506870

Informations de publication

Date de publication:
03 Jan 2023
Historique:
received: 12 07 2022
accepted: 22 11 2022
entrez: 2 1 2023
pubmed: 3 1 2023
medline: 5 1 2023
Statut: epublish

Résumé

Bacillus subtilis strains play a pivotal role in the fermentation industry. B. subtilis phages can cause severe damage by infecting bacterial cells used in industrial fermentation processes. In this work, we isolated and characterized a Bacillus subtilis-infecting phage, termed phi18. Transmission electron microscopy revealed that phage phi18 particles have typical myovirus morphology, with an icosahedral head connected to a contractile tail. Genomic analysis revealed that the phage genome is a linear double-stranded DNA molecule of 147,298 bp with terminal redundancy of 14,434 bp, and 226 protein coding genes and four tRNA genes were predicted in the genome. Phage-resistant mutants were selected from a mariner transposon-insertion library of B. subtilis 168 in which two bacterial genes, tagE and pgcA, which are required for the glycosylation of wall teichoic acid (WTA), were found to be disrupted, suggesting that WTA is the receptor for phage phi18. Comparative genomic analysis showed that phage phi18 is a new member of the genus Okubovirus of the family Herelleviridae. Finally, general characteristics of the phage-resistant mutants, including biofilm formation, growth, and sporulation, were examined. The results showed that the phage-resistant mutants grew as rapidly as the parental strain B. subtilis 168 at 42 °C, suggesting that these phage-resistant mutants may be used as starters in fermentation processes.

Identifiants

pubmed: 36593367
doi: 10.1007/s00705-022-05686-2
pii: 10.1007/s00705-022-05686-2
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

17

Subventions

Organisme : National Natural Science Foundation of China
ID : 31970150

Informations de copyright

© 2022. The Author(s), under exclusive licence to Springer-Verlag GmbH Austria, part of Springer Nature.

Références

Allison SE, D’Elia MA, Arar S, Monteiro MA, Brown ED (2011) Studies of the genetics, function, and kinetic mechanism of TagE, the wall teichoic acid glycosyltransferase in Bacillus subtilis 168. J Biol Chem 286:23708–23716
doi: 10.1074/jbc.M111.241265
Arnaud M, Chastanet A, Débarbouillé M (2004) New vector for efficient allelic replacement in naturally nontransformable, low-GC-content, gram-positive bacteria. Appl Environ Microbiol 70:6887–6891
doi: 10.1128/AEM.70.11.6887-6891.2004
Aziz RK, Bartels D, Best AA, DeJongh M, Disz T, Edwards RA, Formsma K, Gerdes S, Glass EM, Kubal M (2008) The RAST Server: rapid annotations using subsystems technology. BMC Genomics 9:75
doi: 10.1186/1471-2164-9-75
Baptista C, Santos MA, Sao-Jose C (2008) Phage SPP1 reversible adsorption to Bacillus subtilis cell wall teichoic acids accelerates virus recognition of membrane receptor YueB. J Bacteriol 190:4989–4996
doi: 10.1128/JB.00349-08
Bolger A, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics (Oxford, England) 30:2114–2120
doi: 10.1093/bioinformatics/btu170
Cai D, Rao Y, Zhan Y, Wang Q, Chen S (2019) Engineering Bacillus for efficient production of heterologous protein: current progress, challenge and prospect. J Appl Microbiol 126:1632–1642
doi: 10.1111/jam.14192
Checinska A, Paszczynski A, Burbank M (2015) Bacillus and other spore-forming genera: variations in responses and mechanisms for survival. Annu Rev Food Sci Technol 6:351–369
doi: 10.1146/annurev-food-030713-092332
Cui W, Han L, Suo F, Liu Z, Zhou L, Zhou Z (2018) Exploitation of Bacillus subtilis as a robust workhorse for production of heterologous proteins and beyond. World J Microbiol Biotechnol 34:145
doi: 10.1007/s11274-018-2531-7
Cui X, You J, Sun L, Yang X, Zhang T, Huang K, Pan X, Zhang F, He Y, Yang H (2016) Characterization of Pseudomonas aeruginosa phage C11 and identification of host genes required for virion maturation. Sci Rep 6:39130
doi: 10.1038/srep39130
Darzentas N (2010) Circoletto: visualizing sequence similarity with Circos. Bioinformatics 26(20)
Dion MB, Oechslin F, Moineau S (2020) Phage diversity, genomics and phylogeny. Nat Rev Microbiol 18:125–138
doi: 10.1038/s41579-019-0311-5
Dubnau D, Davidoff-Abelson R (1971) Fate of transforming DNA following uptake by competent Bacillus subtilis. I. Formation and properties of the donor-recipient complex. J Mol Biol 56:209–221
doi: 10.1016/0022-2836(71)90460-8
Dunne M, Hupfeld M, Klumpp J, Loessner MJ (2018) Molecular basis of bacterial host interactions by gram-positive targeting bacteriophages. Viruses 10(8):397
Ghosh K, Kang HS, Hyun WB, Kim KP (2018) High prevalence of Bacillus subtilis-infecting bacteriophages in soybean-based fermented foods and its detrimental effects on the process and quality of Cheonggukjang. Food Microbiol 76:196–203
doi: 10.1016/j.fm.2018.05.007
Ghosh K, Kim KP (2019) Complete nucleotide sequence analysis of a novel Bacillus subtilis-infecting phage, BSP38, possibly belonging to a new genus in the subfamily Spounavirinae. Arch Virol 164:875–878
doi: 10.1007/s00705-018-4110-5
Gopal N, Hill C, Ross PR, Beresford TP, Fenelon MA, Cotter PD (2015) The prevalence and control of bacillus and related spore-forming bacteria in the dairy industry. Front Microbiol 6:1418
doi: 10.3389/fmicb.2015.01418
Grin I, Linke D (2011) GCView: the genomic context viewer for protein homology searches. Nucleic Acids Res 39:W353–W356
doi: 10.1093/nar/gkr364
Grose JH, Jensen GL, Burnett SH, Breakwell DP (2014) Genomic comparison of 93 Bacillus phages reveals 12 clusters, 14 singletons and remarkable diversity. BMC Genomics 15:855
doi: 10.1186/1471-2164-15-855
Hagens S, Loessner MJ (2007) Application of bacteriophages for detection and control of foodborne pathogens. Appl Microbiol Biotechnol 76:513–519
doi: 10.1007/s00253-007-1031-8
Hemphill HE, Whiteley HR (1975) Bacteriophages of Bacillus subtilis. Bacteriol Rev 39:257–315
doi: 10.1128/br.39.3.257-315.1975
Klumpp J, Lavigne R, Loessner MJ, Ackermann HW (2010) The SPO1-related bacteriophages. Arch Virol 155:1547–1561
doi: 10.1007/s00705-010-0783-0
Kohm K, Hertel R (2021) The life cycle of SPbeta and related phages. Arch Virol 166:2119–2130
doi: 10.1007/s00705-021-05116-9
Kohm K, Floccari VA, Lutz VT, Nordmann B, Mittelstädt C, Poehlein A, Dragoš A, Commichau FM, Hertel R (2022) The Bacillus phage SPβ and its relatives: a temperate phage model system reveals new strains, species, prophage integration loci, conserved proteins and lysogeny management components. Environ Microbiol 24:2098–2118
doi: 10.1111/1462-2920.15964
Krasowska A, Biegalska A, Augustyniak D, Los M, Richert M, Lukaszewicz M (2015) Isolation and characterization of phages infecting Bacillus subtilis. Biomed Res Int 2015:179597
doi: 10.1155/2015/179597
Lavysh D, Sokolova M, Minakhin L, Yakunina M, Artamonova T, Kozyavkin S, Makarova KS, Koonin EV, Severinov K (2016) The genome of AR9, a giant transducing Bacillus phage encoding two multisubunit RNA polymerases. Virology 495:185–196
doi: 10.1016/j.virol.2016.04.030
Lazarevic V, Soldo B, Médico N, Pooley H, Bron S, Karamata D (2005) Bacillus subtilis alpha-phosphoglucomutase is required for normal cell morphology and biofilm formation. Appl Environ Microbiol 71:39–45
doi: 10.1128/AEM.71.1.39-45.2005
Lee NK, Kim WS, Paik HD (2019) Bacillus strains as human probiotics: characterization, safety, microbiome, and probiotic carrier. Food Sci Biotechnol 28:1297–1305
doi: 10.1007/s10068-019-00691-9
Li L, Yang H, Lin S, Jia S (2010) Classification of 17 newly isolated virulent bacteriophages of Pseudomonas aeruginosa. Can J Microbiol 56:925–933
doi: 10.1139/W10-075
Li R, Zhu H, Ruan J, Qian W, Fang X, Shi Z, Li Y, Li S, Shan G, Kristiansen K, Li S, Yang H, Wang J, Wang J (2010) De novo assembly of human genomes with massively parallel short read sequencing. Genome Res 20:265–272
doi: 10.1101/gr.097261.109
Pan X, Cui X, Zhang F, He Y, Li L, Yang H (2016) Genetic evidence for O-specific antigen as receptor of Pseudomonas aeruginosa phage K8 and its genomic analysis. Front Microbiol 7:252
doi: 10.3389/fmicb.2016.00252
Ritz MP, Perl AL, Colquhoun JM, Chamakura KR, Kuty Everett GF (2013) Complete genome of Bacillus subtilis Myophage CampHawk. Genome Announc 1(6):e00984-13
Ruiz Sella SRB, Bueno T, de Oliveira AAB, Karp SG, Soccol CR (2021) Bacillus subtilis natto as a potential probiotic in animal nutrition. Crit Rev Biotechnol 41:355–369
doi: 10.1080/07388551.2020.1858019
Samson JE, Moineau S (2013) Bacteriophages in food fermentations: new frontiers in a continuous arms race. Annu Rev Food Sci Technol 4:347–368
doi: 10.1146/annurev-food-030212-182541
Setlow P (2001) Resistance of spores of Bacillus species to ultraviolet light. Environ Mol Mutagen 38:97–104
doi: 10.1002/em.1058
Soldo B, Lazarevic V, Margot P, Karamata D (1993) Sequencing and analysis of the divergon comprising gtaB, the structural gene of UDP-glucose pyrophosphorylase of Bacillus subtilis 168. J Gen Microbiol 139:3185–3195
doi: 10.1099/00221287-139-12-3185
Spizizen J (1958) Transformation of biochemically deficient strains of Bacillus subtilis by deoxyribonucleate. Proc Natl Acad Sci 44:1072–1078
doi: 10.1073/pnas.44.10.1072
Stecchini ML, Del Torre M, Polese P (2013) Survival strategies of Bacillus spores in food. Indian J Exp Biol 51:905–909
Steinmetz M, Richter R (1994) Easy cloning of mini-Tn10 insertions from the Bacillus subtilis chromosome. J Bacteriol 176:1761–1763
doi: 10.1128/jb.176.6.1761-1763.1994
Stewart CR, Casjens SR, Cresawn SG, Houtz JM, Smith AL, Ford ME, Peebles CL, Hatfull GF, Hendrix RW, Huang WM, Pedulla ML (2009) The genome of Bacillus subtilis bacteriophage SPO1. J Mol Biol 388:48–70
doi: 10.1016/j.jmb.2009.03.009
Stewart CR, Deery WJ, Egan ES, Myles B, Petti AA (2013) The product of SPO1 gene 56 inhibits host cell division during infection of Bacillus subtilis by bacteriophage SPO1. Virology 447:249–253
doi: 10.1016/j.virol.2013.09.005
Stewart CR (2018) Analysis of host-takeover during SPO1 infection of Bacillus subtilis. Methods Mol Biol 1681:31–39
doi: 10.1007/978-1-4939-7343-9_2
Turner D, Kropinski AM, Adriaenssens EM (2021) A roadmap for genome-based phage taxonomy. Viruses 13:506
doi: 10.3390/v13030506
Umene K, Shiraishi A (2013) Complete nucleotide sequence of Bacillus subtilis (natto) bacteriophage PM1, a phage associated with disruption of food production. Virus Genes 46:524–534
doi: 10.1007/s11262-013-0876-4
Willms IM, Hertel R (2016) Phage vB_BsuP-Goe1: the smallest identified lytic phage of Bacillus subtilis. FEMS Microbiol Lett 363(19):fnw208
Willms IM, Hoppert M, Hertel R (2017) Characterization of Bacillus subtilis viruses vB_BsuM-Goe2 and vB_BsuM-Goe3. Viruses 9(6):146
Yang H, Liang L, Lin S, Jia S (2010) Isolation and characterization of a virulent bacteriophage AB1 of Acinetobacter baumannii. BMC Microbiol 10:131
doi: 10.1186/1471-2180-10-131
Yasbin RE, Maino VC, Young FE (1976) Bacteriophage resistance in Bacillus subtilis 168, W23, and interstrain transformants. J Bacteriol 125:1120–1126
doi: 10.1128/jb.125.3.1120-1126.1976
Yee LM, Matsumoto T, Yano K, Matsuoka S, Sadaie Y, Yoshikawa H, Asai K (2011) The genome of Bacillus subtilis phage SP10: a comparative analysis with phage SPO1. Biosci Biotechnol Biochem 75:944–952
doi: 10.1271/bbb.100921
Young FE (1967) Requirement of glucosylated teichoic acid for adsorption of phage in Bacillus subtilis 168. Proc Natl Acad Sci USA 58:2377–2384
doi: 10.1073/pnas.58.6.2377
Yuan Y, Gao M (2017) Jumbo bacteriophages: an overview. Front Microbiol 8:403
doi: 10.3389/fmicb.2017.00403
Zhang C, Shi L, Yu Y, Yang H (2015) Characterization of a mariner transposon pKKma. Acta Microbiol Sin 55:366–371

Auteurs

Zhiqiang Zhang (Z)

Key Laboratory of Industrial Microbiology of the Ministry of Education, Tianjin Key Laboratory of Industrial Microbiology, College of Biotechnology, Tianjin University of Science and Technology, Tianjin, 300457, China.

Li Liang (L)

Shandong Vland Biotech Co., Ltd, Shandong, 251700, China.

Donghang Li (D)

Key Laboratory of Industrial Microbiology of the Ministry of Education, Tianjin Key Laboratory of Industrial Microbiology, College of Biotechnology, Tianjin University of Science and Technology, Tianjin, 300457, China.

Yutong Li (Y)

Key Laboratory of Industrial Microbiology of the Ministry of Education, Tianjin Key Laboratory of Industrial Microbiology, College of Biotechnology, Tianjin University of Science and Technology, Tianjin, 300457, China.

Qinghui Sun (Q)

Key Laboratory of Tropical Translational Medicine of Ministry of Education, NHC Key Laboratory of Control of Tropical Diseases, School of Tropical Medicine, Hainan Medical University, Hainan, 571199, China.

Ye Li (Y)

Institute of Environment and Plant Protection, Chinese Academy of Tropical Agricultural Sciences, Hainan University, Hainan, 571199, China.

Hongjiang Yang (H)

Key Laboratory of Industrial Microbiology of the Ministry of Education, Tianjin Key Laboratory of Industrial Microbiology, College of Biotechnology, Tianjin University of Science and Technology, Tianjin, 300457, China. hongjiangyang@tust.edu.cn.

Articles similaires

Coal Metagenome Phylogeny Bacteria Genome, Bacterial
Genome, Viral Ralstonia Composting Solanum lycopersicum Bacteriophages
Genome, Bacterial Virulence Phylogeny Genomics Plant Diseases
Host Specificity Bacteriophages Genomics Algorithms Escherichia coli

Classifications MeSH