Low-level predation by lytic phage phiIPLA-RODI promotes biofilm formation and triggers the stringent response in Staphylococcus aureus

Scientific Reports

Volumn 7, Issue , 2017, Pages

  Fernández, Lucía ^a   González, Silvia ^a   Campelo, Ana Belén ^a   Martínez, Beatriz ^a   Rodríguez, Ana ^a   García, Pilar ^a  

^a DEPARTMENT OF MICROBIOLOGY AND BIOCHEMISTRY OF DAIRY PRODUCTS   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL CELL; BIOFILM; DISEASE CARRIER; DNA CONTENT; DNA TRANSCRIPTION; HUMAN; NONHUMAN; PHAGE THERAPY; PREDATOR; STAPHYLOCOCCUS AUREUS; BACTERIOLYSIS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GROWTH, DEVELOPMENT AND AGING; HOST PARASITE INTERACTION; PHYSIOLOGICAL STRESS; PHYSIOLOGY; SEQUENCE ANALYSIS; STAPHYLOCOCCUS PHAGE; VIROLOGY;

BACTERIOLYSIS; BIOFILMS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, BACTERIAL; HOST-PARASITE INTERACTIONS; SEQUENCE ANALYSIS, RNA; STAPHYLOCOCCUS AUREUS; STAPHYLOCOCCUS PHAGES; STRESS, PHYSIOLOGICAL;

EID: 85010298999     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep40965     Document Type: Article

References (58)

1. Koskella, B. & Brockhurst, M. A. Bacteria-phage coevolution as a driver of ecological and evolutionary processes in microbial communities. FEMS Microbiology Reviews 38, 916-931 (2014).
2. Díaz-Muñoz, S. L. & Koskella, B. Bacteria-phage interactions in natural environments. Adv Appl Microbiol 89, 135-183 (2014).
3. Chaturongakul, S. & Ounjai, P. Phage-host interplay: examples from tailed phages and Gram-negative bacterial pathogens. Front Microbiol 5, 442 (2014).
4. Obeng, N., Pratama, A. A. & Elsas, J. D. The significance of mutualistic phages for bacterial ecology and evolution. Trends Microbiol 24, 440-449 (2016).
5. Ainsworth, S., Zomer, A., Mahony, J. & van Sinderen, D. Lytic infection of Lactococcus lactis by bacteriophages Tuc2009 and c2 triggers alternative transcriptional host responses. Appl Environ Microbiol 79, 4786-4798 (2013).
6. Poranen, M. M. et al. Global changes in cellular gene expression during bacteriophage PRD1 infection. J Virol 80, 8081-8088 (2006).
7. Fallico, V., Ross, R. P., Fitzgerald, G. F. & McAuliffe, O. Genetic response to bacteriophage infection in Lactococcus lactis reveals a four-strand approach involving induction of membrane stress proteins, D-Alanylation of the cell wall, maintenance of proton motive force, and energy conservation. J Virol 85, 12032-12042 (2011).
8. Zhao, X. et al. Global transcriptomic analysis of interactions between Pseudomonas aeruginosa and bacteriophage PaP3. Sci Rep 6, 19237 (2016).
9. Lavigne, R. et al. A multifaceted study of Pseudomonas aeruginosa shutdown by virulent podovirus LUZ19. MBio 4, e00061-13 (2013).
10. Kutateladze, M. & Adamia, R. Bacteriophages as potential new therapeutics to replace or supplement antibiotics. Trends Biotechnol 28, 591-595 (2010).
11. Kutter, E. et al. Phage therapy in clinical practice: Treatment of human infections. Curr Pharm Biotechnol 11, 69-86 (2010).
12. Chan, B. K. & Abedon, S. T. Bacteriophages and their enzymes in biofilm control. Curr Pharm Des 21, 85-99 (2015).
13. Gutiérrez, D., Martínez, B., Rodríguez, A. & García, P. Genomic characterization of two Staphylococcus epidermidis bacteriophages with anti-biofilm potential. BMC Genomics 13, 228 (2012).
14. Parasion, S., Kwiatek, M., Gryko, R., Mizak, L. & Malm, A. Bacteriophages as an alternative strategy for fighting biofilm development. Pol J Microbiol 63, 137-145 (2014).
15. Gupta, K., Marques, C. N., Petrova, O. E. & Sauer, K. Antimicrobial tolerance of Pseudomonas aeruginosa biofilms is activated during an early developmental stage and requires the two-component hybrid SagS. J Bacteriol 195, 4975-4987 (2013).
16. Costerton, J. W. et al. Bacterial biofilms in nature and disease. Annu Rev Microbiol 41, 435-464 (1987).
17. de la Fuente-Núñez, C., Reffuveille, F., Fernández, L. & Hancock, R. E. W. Bacterial biofilm development as a multicellular adaptation: Antibiotic resistance and new therapeutic strategies. Curr Opin Microbiol 16, 580-589 (2013).
18. Otto, M. Staphylococcal infections: mechanisms of biofilm maturation and detachment as critical determinants of pathogenicity. Annu Rev Med 64, 175-188 (2013).
19. Lowy, F. D. Antimicrobial resistance: The example of Staphylococcus aureus. J Clin Invest 111, 1265-1273 (2003).
20. Alves, D. R. et al. Combined use of bacteriophage K and a novel bacteriophage to reduce Staphylococcus aureus biofilm formation. Appl Environ Microbiol 80, 6694-6703 (2014).
21. Gutiérrez, D. et al. Two Phages, phiIPLA-RODI and phiIPLA-C1C, Lyse Mono-And Dual-Species Staphylococcal Biofilms. Appl Environ Microbiol 81, 3336-3348 (2015).
22. Kelly, D., McAuliffe, O., Ross, R. P. & Coffey, A. Prevention of Staphylococcus aureus biofilm formation and reduction in established biofilm density using a combination of phage K and modified derivatives. Lett Appl Microbiol 54, 286-291 (2012).
23. Anderson, K. L. et al. Characterization of the Staphylococcus aureus heat shock, cold shock, stringent, and SOS responses and their effects on log-phase mRNA turnover. J Bacteriol 188, 6739-6756 (2006).
24. Reib, S. et al. Global analysis of the Staphylococcus aureus response to mupirocin. Antimicrob Agents Chemother 56, 787-804 (2012).
25. Geiger, T., Kästle, B., Gratani, F. L., Goerke, C. & Wolz, C. Two small (p)ppGpp synthases in Staphylococcus aureus mediate tolerance against cell envelope stress conditions. J Bacteriol 196, 894-902 (2014).
26. Dalebroux, Z. D., Svensson, S. L., Gaynor, E. C. & Swanson, M. S. ppGpp conjures bacterial virulence. Microbiol Mol Biol Rev 74, 171-199 (2010).
27. Maisonneuve, E., Castro-Camargo, M. & Gerdes, K. (p)ppGpp controls bacterial persistence by stochastic induction of toxinantitoxin activity. Cell 154, 1140-1150 (2013).
28. Nguyen, D. et al. Active starvation responses mediate antibiotic tolerance in biofilms and nutrient-limited bacteria. Science 334, 982-986 (2011).
29. Ochi, K., Kandala, J. C. & Freese, E. Initiation of Bacillus subtilis sporulation by the stringent response to partial amino acid deprivation. J Biol Chem 256, 6866-6875 (1981).
30. Gross, M., Cramton, S. E., Götz, F. & Peschel, A. Key role of teichoic acid net charge in Staphylococcus aureus colonization of artificial surfaces. Infect Immun 69, 3423-3426 (2001).
31. Huang, Q., Fei, J., Yu, H. J., Gou, Y. B. & Huang, X. K. Effects of human β-defensin-3 on biofilm formation-regulating genes dltB and icaA in Staphylococcus aureus. Mol Med Rep 10, 825-831 (2014).
32. Koprivnjak, T. et al. Cation-induced transcriptional regulation of the dlt operon of Staphylococcus aureus. J Bacteriol 188, 3622-3630 (2006).
33. Steen, A. et al. Autolysis of Lactococcus lactis is increased upon d-Alanine depletion of peptidoglycan and lipoteichoic acids. J Bacteriol 187, 114-124 (2005).
34. Räisänen, L. et al. Molecular interaction between lipoteichoic acids and Lactobacillus delbrueckii phages depends on d-Alanyl and alpha-glucose substitution of poly(glycerophosphate) backbones. J Bacteriol 189, 4135-4140 (2007).
35. Corrigan, R. M., Bowman, L., Willis, A. R., Kaever, V. & Gröndling, A. Cross-Talk between two nucleotide-signaling pathways in Staphylococcus aureus. J Biol Chem 290, 5826-5839 (2015).
36. Qin, Z. et al. Role of autolysin-mediated DNA release in biofilm formation of Staphylococcus epidermidis. Microbiology 153, 2083-2092 (2007).
37. Houston, P., Rowe, S. E., Pozzi, C., Waters, E. M. & OGara, J. P. Essential role for the major autolysin in the fibronectin-binding protein-mediated Staphylococcus aureus biofilm phenotype. Infect Immun 79, 1153-1165 (2011).
38. Brazas, M. D. & Hancock, R. E. W. Using microarray gene signatures to elucidate mechanisms of antibiotic action and resistance. Drug Discov Today 10, 1245-1252 (2005).
39. Wecke, T. & Mascher, T. Antibiotic research in the age of omics: from expression profiles to interspecies communication. J Antimicrob Chemother 66, 2689-2704 (2011).
40. Otto, M. Staphylococcal biofilms. Curr Top Microbiol Immunol 322, 207-228 (2008).
41. Fernández, L., Breidenstein, E. B. & Hancock, R. E. W. Creeping baselines and adaptive resistance to antibiotics. Drug Resist Updat 14, 1-21 (2011).
42. Fortier, L. C. & Sekulovic, O. Importance of prophages to evolution and virulence of bacterial pathogens. Virulence 4, 354-365 (2013).
43. Gödeke, J., Paul, K., Lassak, J. & Thormann, K. M. Phage-induced lysis enhances biofilm formation in Shewanella oneidensis MR-1. ISME J 5, 613-626 (2011).
44. Carrolo, M., Frias, M. J., Pinto, F. R., Melo-Cristino, J. & Ramirez, M. Prophage spontaneous activation promotes DNA release enhancing biofilm formation in Streptococcus pneumoniae. PLoS One 5, e15678 (2010).
45. Hosseinidoust, Z., Tufenkji, N. & van de Ven, T. G. Formation of biofilms under phage predation: considerations concerning a biofilm increase. Biofouling 29, 457-468 (2013).
46. Tan, D., Dahl, A. & Middelboe, M. Vibriophages differentially influence biofilm formation by Vibrio anguillarum strains. Appl Environ Microbiol 81, 4489-4497 (2015).
47. Webb, J. S. et al. Cell death in Pseudomonas aeruginosa biofilm development. J Bacteriol. 185, 4585-4592 (2003).
48. Leskinen, K., Blasdel, B. G., Lavigne, R. & Skurnik, M. RNA-sequencing reveals the progression of phage-host interactions between φ R1-37 and Yersinia enterocolitica. Freed EO, ed. Viruses. 8, 111 (2016).
49. Aranda, M. & Maule, A. Virus-induced host gene shutoff in animals and plants. Virology 243, 261-267 (1998).
50. Ehrenfeld, E. Poliovirus-induced inhibition of host-cell protein synthesis. Cell 28, 435-436 (1982).
51. de Smet, J. et al. High coverage metabolomics analysis reveals phage-specific alterations to Pseudomonas aeruginosa physiology during infection. ISME J. doi: 10.1038/ismej.2016.3 (2016).
52. Gutiérrez, D. et al. Incidence of Staphylococcus aureus and analysis of associated bacterial communities on food industry surfaces. Appl Environ Microbiol 78, 8547-8554 (2012).
53. Herrera, J. J., Cabo, M. L., González, A., Pazos, I. & Pastoriza, L. Adhesion and detachment kinetics of several strains of Staphylococcus aureus subsp. aureus under three different experimental conditions. Food Microbiol 24, 585-591 (2007).
54. Gutiérrez, D., Ruas-Madiedo, P., Martínez, B., Rodríguez, A. & García, P. Effective removal of staphylococcal biofilms by the endolysin LysH5. PLoS One 9, e107307 (2014).
55. Kaplan, J. B. et al. Low levels of β-lactam antibiotics induce extracellular DNA release and biofilm formation in Staphylococcus aureus. MBio 3, e00198-12 (2012).
56. Dougherty, P. F., Yotter, D. W. & Matthews, T. R. Microdilution transfer plate technique for determining in vitro synergy of antimicrobial agents. Antimicrob Agents Chemother 11, 225-228 (1977).
57. Clinical and Laboratory Standards Institute. M7-A7. Methods for dilution antimicrobial susceptibility tests for bacteria that grow aerobically; Approved Standard-7th ed. (Clinical and Laboratory Standards Institute, 2006).
58. Clinical and Laboratory Standards Institute. M100-S17. Performance standards for antimicrobial susceptibility testing; Approved Standard-17th ed. (Clinical and Laboratory Standards Institute, 2007).