Spatial vulnerability: Bacterial arrangements, microcolonies, and biofilms as responses to low rather than high phage densities

Viruses

Volumn 4, Issue 5, 2012, Pages 663-687

  Abedon, Stephen T ^a  

^a OHIO STATE UNIVERSITY   (United States)

Author keywords

Adsorption; Bacteriophage; Biofilms; Cellular arrangements; Ecology; Microcolonies; Particle transport; Phage therapy; Phages

Indexed keywords

ADSORPTION KINETICS; ARTICLE; BACTERIAL GROWTH; BACTERIAL SURVIVAL; BACTERIAL VIRULENCE; BACTERIOPHAGE; BACTERIUM COLONY; BIOFILM; CELL DENSITY; CELL TRANSPORT; CLONAL VARIATION; CONTROLLED STUDY; COST BENEFIT ANALYSIS; ENVIRONMENTAL FACTOR; MATHEMATICAL COMPUTING; MATHEMATICAL MODEL; MOLECULAR CLONING; MOLECULAR DYNAMICS; MOLECULAR SIZE; NONHUMAN; PARTICLE SIZE; POPULATION DENSITY; PREDICTION; PRESSURE MEASUREMENT; VIRUS CELL INTERACTION;

BACTERIA; BACTERIAL PHYSIOLOGICAL PHENOMENA; BACTERIOPHAGES; BIOFILMS; HOST-PARASITE INTERACTIONS; MICROBIAL VIABILITY; MODELS, STATISTICAL;

BACTERIA (MICROORGANISMS);

EID: 84861553731     PISSN: None     EISSN: 19994915     Source Type: Journal    
DOI: 10.3390/v4050663     Document Type: Article

References (75)

1. Stoodley, P.; Sauer, K.; Davies, D.G.; Costerton, J.W. Biofilms as complex differentiated communities. Ann. Rev. Microbiol. 2002, 56, 187-209.
2. Kjelleberg, S.; Givskov, M. The Biofilm Mode of Life: Mechanisms and Adaptations; Horizon Biosciences: Norfolk, UK, 2007.
3. Ramage, G.; Culshaw, S.; Jones, B.; Williams, C. Are we any closer to beating the biofilm: Novel methods of biofilm control. Curr. Opin. Infect. Dis. 2010, 23, 560-566.
4. Gino, E.; Starosvetsky, J.; Kurzbaum, E.; Armon, R. Combined chemical-biological treatment for prevention/rehabilitation of clogged wells by an iron-oxidizing bacterium. Environ. Sci. Technol. 2010, 44, 3123-3129.
5. Cos, P.; Tote, K.; Horemans, T.; Maes, L. Biofilms: An extra hurdle for effective antimicrobial therapy. Curr. Pharm. Des. 2010, 16, 2279-2295.
6. Abedon, S.T. Kinetics of phage-mediated biocontrol of bacteria. Foodborne Pathog. Dis. 2009, 6, 807-815.
7. Loc-Carrillo, C.; Abedon, S.T. Pros and cons of phage therapy. Bacteriophage 2011, 1, 111-114.
8. Abedon, S.T. Bacteriophages and biofilms. In Biofilms: Formation, Development and Properties; Bailey, W.C., Ed.; Nova Science Publishers: Hauppauge, NY, USA, 2010; Chapter 1, pp. 1-58.
9. Abedon, S.T. Bacteriophages and Biofilms: Ecology, Phage Therapy, Plaques; Nova Science Publishers: Hauppauge, NY, USA, 2011.
10. Abedon, S.T.; Thomas-Abedon, C.; Thomas, A.; Mazure, H. Bacteriophage prehistory: Is or is not Hankin, 1896, a phage reference? Bacteriophage 2011, 1, 174-178.
11. Twort, F.W. An investigation on the nature of ultra-microscopic viruses. Lancet 1915, ii, 1241-1243.
12. Twort, F.W. An investigation on the nature of ultra-microscopic viruses. Bacteriophage 2011, 1, 127-129.
13. Abedon, S.T.; Yin, J. Impact of spatial structure on phage population growth. In Bacteriophage Ecology; Abedon, S.T., Ed.; Cambridge University Press: Cambridge, UK, 2008; Volume 15, Chapter 4, pp. 94-113.
14. Krone, S.M.; Abedon, S.T. Modeling phage plaque growth. In Bacteriophage Ecology; Abedon, S.T., Ed.; Cambridge University Press: Cambridge, UK, 2008; Volume 15, Chapter 16, pp. 415-438.
15. Abedon, S.T.; Yin, J. Bacteriophage plaques: Theory and analysis. Meth. Mol. Biol. 2009, 501, 161-174.
16. Gallet, R.; Shao, Y.; Wang, I.N. High adsorption rate is detrimental to bacteriophage fitness in a biofilm-like environment. BMC Evol. Biol. 2009, 9, 241.
17. Gallet, R.; Kannoly, S.; Wang, I.N. Effects of bacteriophage traits on plaque formation. BMC Microbiol. 2011, 11, 181.
18. Abedon, S.T. Communication among phages, bacteria, and soil environments. In Biocommunication of Soil Microorganisms; Witzany, G., Ed.; Springer: New York, NY, USA, 2011; Volume 23, Chapter 2, pp. 37-65.
19. Abedon, S.T.; Thomas-Abedon, C. Phage therapy pharmacology. Curr. Pharm. Biotechnol. 2010, 11, 28-47.
20. Gill, J.J.; Hyman, P. Phage choice, isolation and preparation for phage therapy. Curr. Pharm. Biotechnol. 2010, 11, 2-14.
21. Lu, T.K.; Collins, J.J. Dispersing biofilms with engineered enzymatic bacteriophage. Proc. Natl. Acad. Sci. U. S. A. 2007, 104, 11197-11202.
22. Goodridge, L.D. Designing phage therapeutics. Curr. Pharm. Biotechnol. 2010, 11, 15-27.
23. Mondes, R.; O'Toole, G.A. The developmental model of microbial biofilms: Ten years of a paradigm up for review. Trends Microbiol. 2009, 17, 73-87.
24. Murray, A.G.; Jackson, G.A. Viral dynamics: A model of the effects of size, shape, motion, and abundance of single-celled planktonic organisms and other particles. Mar. Ecol. Prog. Ser. 1992, 89, 103-116.
25. Abedon, S. Phage therapy pharmacology: Calculating phage dosing. Adv. Appl. Microbiol. 2011, 77, 1-40.
26. Thingstad, T.F. Elements of a theory for the mechanisms controlling abundance, diversity, and biogeochemical role of lytic bacterial viruses in aquatic systems. Limnol. Oceanogr. 2000, 45, 1320-1328.
27. Thingstad, T.F.; Bratbak, G.; Heldal, M. Aquatic phage ecology. In Bacteriophage Ecology; Abedon, S.T., Ed.; Cambridge University Press: Cambridge, UK, 2008; Chapter 10, pp. 251-280.
28. Chao, L.; Levin, B.R.; Stewart, F.M. A complex community in a simple habitat: An experimental study with bacteria and phage. Ecology 1977, 58, 369-378.
29. Schrag, S.; Mittler, J.E. Host-parasite persistence: The role of spatial refuges in stabilizing bacteria-phage interactions. Am. Nat. 1996, 148, 348-377.
30. Hyman, P.; Abedon, S.T. Bacteriophage host range and bacterial resistance. Adv. Appl. Microbiol. 2010, 70, 217-248.
31. Labrie, S.J.; Samson, J.E.; Moineau, S. Bacteriophage resistance mechanisms. Nat. Rev. Microbiol. 2010, 8, 317-327.
32. Abedon, S.T. Bacterial 'immunity' against bacteriophages. Bacteriophage 2012, 2, 50-54.
33. Abedon, S.T. Lysis of lysis inhibited bacteriophage T4-infected cells. J. Bacteriol. 1992, 174, 8073-8080.
34. Abedon, S.T. Envisaging bacteria as phage targets. Bacteriophage 2011, 1, 228-230.
35. Stent, G.S. Molecular Biology of Bacterial Viruses; WH Freeman and Co.: San Francisco, CA, USA, 1963.
36. Ioannou, C.C.; Bartumeus, F.; Krause, J.; Ruxton, G.D. Unified effects of aggregation reveal larger prey groups take longer to find. Proc. Biol. Sci 2011, 278, 2985-2990.
37. Abedon, S.T. Phage population growth: Constraints, games, adaptation. In Bacteriophage Ecology; Abedon, S.T., Ed.; Cambridge University Press: Cambridge, UK, 2008; Volume 15, Chapter 3, pp. 64-93.
38. Kasman, L.M.; Kasman, A.; Westwater, C.; Dolan, J.; Schmidt, M.G.; Norris, J.S. Overcoming the phage replication threshold: A mathematical model with implications for phage therapy. J. Virol. 2002, 76, 5557-5564.
39. Abedon, S.T. Bacteriophage T4 resistance to lysis-inhibition collapse. Genet. Res. 1999, 74, 1-11.
40. Young, K.D. The selective value of bacterial shape. Microbiol. Mol. Biol. Rev. 2006, 70, 660-703.
41. Young, K.D. Bacterial morphology: Why have different shapes? Curr. Opin. Microbiol. 2007, 10, 596-600.
42. Azeredo, J.; Sutherland, I.W. The use of phages for the removal of infectious biofilms. Curr. Pharm. Biotechnol. 2008, 9, 261-266.
43. Turner, G.F.; Pitcher, T.J. Attack abatement: A model for group protection by combined avoidance and dilution. Am. Nat. 1986, 128, 228-240.
44. Babic, A.; Berkmen, M.B.; Lee, C.A.; Grossman, A.D. Efficient gene transfer in bacterial cell chains. MBio 2011, 2, e00027-11.
45. Abedon, S.T. Phages, ecology, evolution. In Bacteriophage Ecology; Abedon, S.T., Ed.; Cambridge University Press: Cambridge, UK, 2008; Volume 15, Chapter 1, pp. 1-28.
46. Hagens, S.; Loessner, M.J. Bacteriophage for biocontrol of foodborne pathogens: Calculations and considerations. Curr. Pharm. Biotechnol. 2010, 11, 58-68.
47. Goodridge, L.D. Phages, bacteria, and food. In Bacteriophage Ecology; Abedon, S.T., Ed.; Cambridge University Press: Cambridge, UK, 2008; Chapter 12, pp. 302-331.
48. Xavier, J.B.; Foster, K.R. Cooperation and conflict in microbial biofilms. Proc. Natl. Acad. Sci. U. S. A. 2007, 104, 876-881.
49. Wimpenny, J. Ecological determinants of biofilm formation. Biofouling 1996, 10, 43-63.
50. Nadell, C.D.; Xavier, J.B.; Levin, S.A.; Foster, K.R. The evolution of quorum sensing in bacterial biofilms. PLoS Biol. 2008, 6, e14.
51. Crombach, A.; Hogeweg, P. Evolution of resource cycling in ecosystems and individuals. BMC Evol. Biol. 2009, 9, 122.
52. Hoffmeister, M.; Martin, W. Interspecific evolution: Microbial symbiosis, endosymbiosis and gene transfer. Environ. Microbiol. 2003, 5, 641-649.
53. Searcy, D.G. Metabolic integration during the evolutionary origin of mitochondria. Cell Res. 2003, 13, 229-238.
54. Kreft, J.U. Biofilms promote altruism. Microbiology 2004, 150, 2751-2760.
55. Nadell, C.D.; Bassler, B.L. A fitness trade-off between local competition and dispersal in Vibrio cholerae biofilms. Proc. Natl. Acad. Sci U. S. A. 2011, 108, 14181-14185.
56. Takahashi, N.; Nyvad, B. The role of bacteria in the caries process: Ecological perspectives. J. Dent. Res. 2011, 90, 294-303.
57. Kolter, R. Biofilms in lab and nature: A molecular geneticist's voyage to microbial ecology. Int. Microbiol. 2010, 13, 1-7.
58. Whiteley, M.; Ott, J.R.; Weaver, E.A.; McLean, R.J.C. Effects of community composition and growth rate on aquifer biofilm bacteria and their susceptibility to betadine disinfection. Environ. Microbiol. 2001, 3, 43-52.
59. Matz, C. Biofilms as refuge against predation. In The Biofilm Mode of Life: Mechanisms and Adaptations; Kjelleberg, S., Givskov, M., Eds.; Horizon Bioscience: Norfolk, UK, 2007; Chapter 11, pp. 195-213.
60. Thurlow, L.R.; Hanke, M.L.; Fritz, T.; Angle, A.; Aldrich, A.; Williams, S.H.; Engebretsen, I.L.; Bayles, K.W.; Horswill, A.R.; Kielian, T. Staphylococcus aureus biofilms prevent macrophage phagocytosis and attenuate inflammation in vivo. J. Immunol. 2011, 186, 6585-6596.
61. Arciola, C.R. Host defense against implant infection: The ambivalent role of phagocytosis. Int. J. Artif. Organs 2010, 33, 565-567.
62. Jensen, P.O.; Givskov, M.; Bjarnsholt, T.; Moser, C. The immune system vs. Pseudomonas aeruginosa biofilms. FEMS Immunol. Med. Microbiol. 2010, 59, 292-305.
63. Costerton, J.W.; Cheng, J.-J.; Geesey, G.G.; Ladd, T.I.; Nickel, J.C.; Dasgupta, M.; Marrie, T.J. Bacterial biofilms in nature and disease. Ann. Rev. Microbiol. 1987, 41, 435-464.
64. Barron, B.A.; Fischetti, V.A.; Zabriskie, J.B. Studies of the bacteriophage kinetics of multicellular systems: A statistical model for the estimation of burst size per cell in streptococci. J. Appl. Bacteriol. 1970, 33, 436-442.
65. Friend, P.L.; Slade, A.D. Characteristics of group A streptococcal bacteriophages. J. Bacteriol. 1966, 92, 148-154.
66. Fischetti, V.A.; Barron, B.; Zabriskie, J.B. Studies on streptococcal bacteriophages. I. burst size and intracellular growth of group A and group C streptococcal bacteriophages. J. Exp. Med. 1968, 127, 475-488.
67. Kaplan, D.A.; Naumovski, L.; Rothschild, B.; Collier, R.J. Appendix: A model of plaque formation. Gene 1981, 13, 221-225.
68. Doolittle, M.M.; Cooney, J.J.; Caldwell, D.E. Tracing the interaction of bacteriophage with bacterial biofilms using fluorescent and chromogenic probes. J. Indust. Microbiol. 1996, 16, 331-341.
69. Abedon, S.T. Bacteriophage intraspecific cooperation and defection. In Contemporary Trends in Bacteriophage Research; Adams, H.T., Ed.; Nova Science Publishers: Hauppauge, NY, USA, 2009; Chapter 7, pp. 191-215.
70. Bohannan, B.J.M.; Lenski, R.E. Effect of prey heterogeneity on the response of a food chain to resource enrichment. Am. Nat. 1999, 153, 73-82.
71. Bohannan, B.J.M.; Lenski, R.E. Linking genetic change to community evolution: Insights from studies of bacteria and bacteriophage. Ecol. Lett. 2000, 3, 362-377.
72. Terborgh, J.; Lopez, L.; Nunez, V.; Rao, M.; Shahabuddin, G.; Orihuela, G.; Riveros, M.; Ascanio, R.; Adler, G.H.; Lambert, T.D.; Balbas, L. Ecological meltdown in predator-free forest fragments. Science 2001, 294, 1923-1926.
73. Abedon, S.T. Phage evolution and ecology. Adv. Appl. Microbiol. 2009, 67, 1-45.
74. Kutter, E.; De Vos, D.; Gvasalia, G.; Alavidze, Z.; Gogokhia, L.; Kuhl, S.; Abedon, S.T. Phage therapy in clinical practice: Treatment of human infections. Curr. Pharm. Biotechnol. 2010, 11, 69-86.
75. Abedon, S.T.; Kuhl, S.J.; Blasdel, B.G.; Kutter, E.M. Phage treatment of human infections. Bacteriophage 2011, 1, 66-85.