1887

Abstract

ssRNA bacteriophages are very abundant but poorly studied, particularly in relation to their effect on bacterial evolution. We isolated a new levivirus, vB_PaeL_PcyII-10_LeviOr01, from hospital waste water. Its genome comprises 3669 nucleotides and encodes four putative proteins. Following bacterial infection, a carrier state is established in a fraction of the cells, conferring superinfection immunity. Such cells also resist other phages that use type IV pili as a receptor. The carrier population is composed of a mixture of cells producing phage, and susceptible cells that are non-carriers. Carrier cells accumulate phage until they burst, releasing large quantities of virions. The continuous presence of phage favours the emergence of host variants bearing mutations in genes involved in type IV pilus biogenesis, but also in genes affecting lipopolysaccharide (LPS) synthesis. The establishment of a carrier state in which phage particles are continuously released was previously reported for some dsRNA phages, but has not previously been described for a levivirus. The present results highlight the importance of the carrier state, an association that benefits both phages and bacteria and plays a role in bacterial evolution.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/jgv.0.000883
2017-08-01
2020-09-25
Loading full text...

Full text loading...

/deliver/fulltext/jgv/98/8/2181.html?itemId=/content/journal/jgv/10.1099/jgv.0.000883&mimeType=html&fmt=ahah

References

  1. Ne Z. RNA Phages Cold Spring Harbor, NY: Cold Spring Harbor Laboratory; 1975
    [Google Scholar]
  2. van Duin J, Tsareva N. Single-stranded RNA phages. In Calendar R, Abedon S. (editors) The Bacteriophages, 2nd ed. New York, NY: Oxford University Press; 2004; pp.175–196
    [Google Scholar]
  3. Friedman SD, Genthner FJ, Gentry J, Sobsey MD, Vinjé J. Gene mapping and phylogenetic analysis of the complete genome from 30 single-stranded RNA male-specific coliphages (family Leviviridae). J Virol 2009;83:11233–11243 [CrossRef][PubMed]
    [Google Scholar]
  4. Loeb T. Isolation of a bacteriophage specific for the F plus and Hfr mating types of Escherichia coli K-12. Science 1960;131:932–933 [CrossRef][PubMed]
    [Google Scholar]
  5. Zinder ND. Portraits of viruses: RNA phage. Intervirology 1980;13:257–270 [CrossRef][PubMed]
    [Google Scholar]
  6. Young R. Bacteriophage lysis: mechanism and regulation. Microbiol Rev 1992;56:430–481[PubMed]
    [Google Scholar]
  7. Bradley DE. The structure and infective process of a Pseudomonas aeruginosa bacteriophage containing ribonucleic acid. J Gen Microbiol 1966;45:83–96 [CrossRef]
    [Google Scholar]
  8. Olsthoorn RC, Garde G, Dayhuff T, Atkins JF, van Duin J. Nucleotide sequence of a single-stranded RNA phage from Pseudomonas aeruginosa: kinship to coliphages and conservation of regulatory RNA structures. Virology 1995;206:611–625 [CrossRef][PubMed]
    [Google Scholar]
  9. Olsen RH, Thomas DD. Characteristics and purification of PRR1, an RNA phage specific for the broad host range Pseudomonas R1822 drug resistance plasmid. J Virol 1973;12:1560–1567[PubMed]
    [Google Scholar]
  10. Ruokoranta TM, Grahn AM, Ravantti JJ, Poranen MM, Bamford DH. Complete genome sequence of the broad host range single-stranded RNA phage PRR1 places it in the Levivirus genus with characteristics shared with Alloleviviruses. J Virol 2006;80:9326–9330 [CrossRef][PubMed]
    [Google Scholar]
  11. Sepúlveda-Robles O, Kameyama L, Guarneros G. High diversity and novel species of Pseudomonas aeruginosa bacteriophages. Appl Environ Microbiol 2012;78:4510–4515 [CrossRef][PubMed]
    [Google Scholar]
  12. Brockhurst MA, Buckling A, Rainey PB. The effect of a bacteriophage on diversification of the opportunistic bacterial pathogen, Pseudomonas aeruginosa. Proc Biol Sci 2005;272:1385–1391 [CrossRef][PubMed]
    [Google Scholar]
  13. Bradley DE. The adsorption of Pseudomonas aeruginosa pilus-dependent bacteriophages to a host mutant with nonretractile pili. Virology 1974;58:149–163 [CrossRef][PubMed]
    [Google Scholar]
  14. Davern CI. The isolation and oharacterization of an rna bacteriophage. Aust J Biol Sci 1964;17:719–725 [CrossRef]
    [Google Scholar]
  15. Romantschuk M, Bamford DH. φ6-resistant phage-producing mutants of Pseudomonas phaseolicola. J Gen Virol 1981;56:287–295 [CrossRef][PubMed]
    [Google Scholar]
  16. Onodera S, Olkkonen VM, Gottlieb P, Strassman J, Qiao XY et al. Construction of a transducing virus from double-stranded RNA bacteriophage phi6: establishment of carrier states in host cells. J Virol 1992;66:190–196[PubMed]
    [Google Scholar]
  17. Siringan P, Connerton PL, Cummings NJ, Connerton IF. Alternative bacteriophage life cycles: the carrier state of Campylobacter jejuni. Open Biol 2014;4:130200 [CrossRef][PubMed]
    [Google Scholar]
  18. Brathwaite KJ, Siringan P, Connerton PL, Connerton IF. Host adaption to the bacteriophage carrier state of Campylobacter jejuni. Res Microbiol 2015;166:504–515 [CrossRef][PubMed]
    [Google Scholar]
  19. Díaz-Muñoz SL, Koskella B. Bacteria-phage interactions in natural environments. Adv Appl Microbiol 2014;89:135–183 [CrossRef][PubMed]
    [Google Scholar]
  20. Jones LM, Mcduff CR, Wilson JB. Phenotypic alterations in the colonial morphology of Brucella abortus due to a bacteriophage carrier state. J Bacteriol 1962;83:860–866[PubMed]
    [Google Scholar]
  21. Li K, Barksdale L, Garmise L. Phenotypic alterations associated with the bacteriophage carrier state of Shigella dysenteriae. J Gen Microbiol 1961;24:355–367 [CrossRef][PubMed]
    [Google Scholar]
  22. Latino L, Midoux C, Hauck Y, Vergnaud G, Pourcel C. Pseudolysogeny and sequential mutations build multiresistance to virulent bacteriophages in Pseudomonas aeruginosa. Microbiology 2016;162:748–763 [CrossRef][PubMed]
    [Google Scholar]
  23. Dai X, Li Z, Lai M, Shu S, du Y et al. In situ structures of the genome and genome-delivery apparatus in a single-stranded RNA virus. Nature 2017;541:112–116 [CrossRef][PubMed]
    [Google Scholar]
  24. Kropinski AM, Prangishvili D, Lavigne R. Position paper: the creation of a rational scheme for the nomenclature of viruses of Bacteria and Archaea. Environ Microbiol 2009;11:2775–2777 [CrossRef][PubMed]
    [Google Scholar]
  25. Cuppels DA, Vidaver AK, van Etten JL. Resistance to bacteriophage φ6 by Pseudomonas phaseolicola. J Gen Virol 1979;44:493–504 [CrossRef]
    [Google Scholar]
  26. Köhler T, Curty LK, Barja F, van Delden C, Pechère JC. Swarming of Pseudomonas aeruginosa is dependent on cell-to-cell signaling and requires flagella and pili. J Bacteriol 2000;182:5990–5996 [CrossRef][PubMed]
    [Google Scholar]
  27. Déziel E, Lépine F, Milot S, Villemur R. rhlA is required for the production of a novel biosurfactant promoting swarming motility in Pseudomonas aeruginosa: 3-(3-hydroxyalkanoyloxy)alkanoic acids (HAAs), the precursors of rhamnolipids. Microbiology 2003;149:2005–2013 [CrossRef][PubMed]
    [Google Scholar]
  28. Overhage J, Lewenza S, Marr AK, Hancock RE. Identification of genes involved in swarming motility using a Pseudomonas aeruginosa PAO1 mini-Tn5-lux mutant library. J Bacteriol 2007;189:2164–2169 [CrossRef][PubMed]
    [Google Scholar]
  29. Chiang P, Burrows LL. Biofilm formation by hyperpiliated mutants of Pseudomonas aeruginosa. J Bacteriol 2003;185:2374–2378 [CrossRef][PubMed]
    [Google Scholar]
  30. Martin PR, Hobbs M, Free PD, Jeske Y, Mattick JS. Characterization of pilQ, a new gene required for the biogenesis of type 4 fimbriae in Pseudomonas aeruginosa. Mol Microbiol 1993;9:857–868 [CrossRef][PubMed]
    [Google Scholar]
  31. Koo J, Tang T, Harvey H, Tammam S, Sampaleanu L et al. Functional mapping of PilF and PilQ in the Pseudomonas aeruginosa type IV pilus system. Biochemistry 2013;52:2914–2923 [CrossRef][PubMed]
    [Google Scholar]
  32. Chiang P, Sampaleanu LM, Ayers M, Pahuta M, Howell PL et al. Functional role of conserved residues in the characteristic secretion NTPase motifs of the Pseudomonas aeruginosa type IV pilus motor proteins PilB, PilT and PilU. Microbiology 2008;154:114–126 [CrossRef][PubMed]
    [Google Scholar]
  33. Wolfgang MC, Lee VT, Gilmore ME, Lory S. Coordinate regulation of bacterial virulence genes by a novel adenylate cyclase-dependent signaling pathway. Dev Cell 2003;4:253–263 [CrossRef][PubMed]
    [Google Scholar]
  34. Schwartz FM, Zinder ND. Crystalline aggregates in bacterial cells infected with the rna bacteriophage f2. Virology 1963;21:276–278 [CrossRef][PubMed]
    [Google Scholar]
  35. Barksdale L, Arden SB. Persisting bacteriophage infections, lysogeny, and phage conversions. Annu Rev Microbiol 1974;28:265–299[CrossRef]
    [Google Scholar]
  36. Hunter GJ. Phage-resistant and phage-carrying strains of lactic streptococci. J Hyg 1947;45:307–312 [CrossRef][PubMed]
    [Google Scholar]
  37. Lwoff A. Lysogeny. Bacteriol Rev 1953;17:269–337[PubMed]
    [Google Scholar]
  38. Bastías R, Higuera G, Sierralta W, Espejo RT. A new group of cosmopolitan bacteriophages induce a carrier state in the pandemic strain of Vibrio parahaemolyticus. Environ Microbiol 2010;12:990–1000 [CrossRef][PubMed]
    [Google Scholar]
  39. Jain R, Srivastava R. Metabolic investigation of host/pathogen interaction using MS2-infected Escherichia coli. BMC Syst Biol 2009;3:121 [CrossRef][PubMed]
    [Google Scholar]
  40. Berzin V, Rosenthal G, Gren EJ. Cellular macromolecule synthesis in Escherichia coli infected with bacteriophage MS2. Eur J Biochem 1974;45:233–242 [CrossRef][PubMed]
    [Google Scholar]
  41. Ravantti JJ, Ruokoranta TM, Alapuranen AM, Bamford DH. Global transcriptional responses of Pseudomonas aeruginosa to phage PRR1 infection. J Virol 2008;82:2324–2329 [CrossRef][PubMed]
    [Google Scholar]
  42. Roine E, Nunn DN, Paulin L, Romantschuk M. Characterization of genes required for pilus expression in Pseudomonas syringae pathovar phaseolicola. J Bacteriol 1996;178:410–417 [CrossRef][PubMed]
    [Google Scholar]
  43. Sistrom M, Park D, O'Brien HE, Wang Z, Guttman DS et al. Genomic and gene-expression comparisons among phage-resistant type-IV pilus mutants of Pseudomonas syringae pathovar phaseolicola. PLoS One 2015;10:e0144514 [CrossRef][PubMed]
    [Google Scholar]
  44. Essoh C, Latino L, Midoux C, Blouin Y, Loukou G et al. Investigation of a large collection of Pseudomonas aeruginosa bacteriophages collected from a single environmental source in Abidjan, Côte d'Ivoire. PLoS One 2015;10:e0130548 [CrossRef][PubMed]
    [Google Scholar]
  45. Pourcel C, Midoux C, Hauck Y, Vergnaud G, Latino L. Large Preferred Region for packaging of bacterial DNA by phiC725A, a novel Pseudomonas aeruginosa F116-like bacteriophage. PLoS One 2017;12:e0169684 [CrossRef][PubMed]
    [Google Scholar]
  46. Kropinski AM, Mazzocco A, Waddell TE, Lingohr E, Johnson RP. Enumeration of bacteriophages by double agar overlay plaque assay. Methods Mol Biol 2009;501:69–76 [CrossRef][PubMed]
    [Google Scholar]
  47. Latino L, Essoh C, Blouin Y, Vu Thien H, Pourcel C. A novel Pseudomonas aeruginosa bacteriophage, Ab31, a chimera formed from temperate phage PAJU2 and P. putida lytic phage AF: characteristics and mechanism of bacterial resistance. PLoS One 2014;9:e93777 [CrossRef][PubMed]
    [Google Scholar]
  48. Hyman P, Abedon ST. Practical methods for determining phage growth parameters. Methods Mol Biol 2009;501:175–202 [CrossRef][PubMed]
    [Google Scholar]
  49. Essoh C, Blouin Y, Loukou G, Cablanmian A, Lathro S et al. The susceptibility of Pseudomonas aeruginosa strains from cystic fibrosis patients to bacteriophages. PLoS One 2013;8:e60575 [CrossRef][PubMed]
    [Google Scholar]
  50. Kellenberger E, Ryter A, Sechaud J. Electron microscope study of DNA-containing plasms. II. Vegetative and mature phage DNA as compared with normal bacterial nucleoids in different physiological states. J Biophys Biochem Cytol 1958;4:671–678 [CrossRef][PubMed]
    [Google Scholar]
  51. Hitchcock PJ, Brown TM. Morphological heterogeneity among Salmonella lipopolysaccharide chemotypes in silver-stained polyacrylamide gels. J Bacteriol 1983;154:269–277[PubMed]
    [Google Scholar]
  52. Fomsgaard A, Freudenberg MA, Galanos C. Modification of the silver staining technique to detect lipopolysaccharide in polyacrylamide gels. J Clin Microbiol 1990;28:2627–2631[PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/jgv.0.000883
Loading
/content/journal/jgv/10.1099/jgv.0.000883
Loading

Data & Media loading...

Supplements

Supplementary File 1

PDF

Most cited this month Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error