Spatial Vulnerability: Bacterial Arrangements, Microcolonies, and Biofilms as Responses to Low Rather than High Phage Densities
Abstract
:1. Introduction
2. Results and Discussion
2.1. Phage Adsorption to Free Bacteria
2.1.1. Phage Movement towards Bacterial Targets
2.1.2. Basic Adsorption Calculations
2.2. Phage Interaction with Bacterial Arrangements
2.2.1. Increased Target Size
2.2.2. Increased Multiplicity of Adsorption
2.2.3. Phage Propagation within Arrangements
2.2.4. Inefficiencies in Phage Propagation
2.2.5. An Important Special Case
Environmental Phage Density (P) | Phage Propagation Ability Through Arrangements ( ) | |||
---|---|---|---|---|
Higher | Lower | |||
Higher (bacterial losses dominate dynamics) | For [lesser or no impediments to phage propagation within arrangements] | For [impediments less than absolute] | For [e.g., abortive infections] | For [e.g., phage restriction] |
Lower (bacterial gains dominate dynamics) | For [which, as P → 0, is more likely] | [assuming phage-independent advantages to arrangement formation, i.e., μA - μN > 0, and that μA - μN > P( -k)holds, which is likely given both P → 0 and → 0] |
2.3. Utility of Group Living in Light of Phages
2.3.1. Selective Benefits of Living in Arrangements
2.3.2. Susceptibility of Bacterial Arrangements and Microcolonies to Phage Exploitation
2.3.3. Phage-Mediated Costs of Existing as Arrangements
2.3.4. Importance of Reduced Vulnerability to Phages
2.3.5. Reduced Bacterial Densities as Phage-Resistance Strategy
3. Experimental Section
4. Conclusions
Acknowledgments
Conflict of Interest
References and Notes
- Stoodley, P.; Sauer, K.; Davies, D.G.; Costerton, J.W. Biofilms as complex differentiated communities. Ann. Rev. Microbiol. 2002, 56, 187–209. [Google Scholar]
- Kjelleberg, S.; Givskov, M. The Biofilm Mode of Life: Mechanisms and Adaptations; Horizon Biosciences: Norfolk, UK, 2007. [Google Scholar]
- 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. [Google Scholar]
- 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. [Google Scholar]
- Cos, P.; Tote, K.; Horemans, T.; Maes, L. Biofilms: An extra hurdle for effective antimicrobial therapy. Curr. Pharm. Des. 2010, 16, 2279–2295. [Google Scholar]
- Abedon, S.T. Kinetics of phage-mediated biocontrol of bacteria. Foodborne Pathog. Dis. 2009, 6, 807–815. [Google Scholar]
- Loc-Carrillo, C.; Abedon, S.T. Pros and cons of phage therapy. Bacteriophage 2011, 1, 111–114. [Google Scholar]
- Abedon, S.T. Bacteriophages and biofilms. In Biofilms: Formation, Development and Properties; Bailey, W.C., Ed.; Nova Science Publishers: Hauppauge, NY, USA, 2010; pp. 1–58, Chapter 1. [Google Scholar]
- Abedon, S.T. Bacteriophages and Biofilms: Ecology, Phage Therapy, Plaques; Nova Science Publishers: Hauppauge, NY, USA, 2011. [Google Scholar]
- 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. [Google Scholar] [CrossRef]
- Twort, F.W. An investigation on the nature of ultra-microscopic viruses. Lancet 1915, ii, 1241–1243. [Google Scholar]
- Twort, F.W. An investigation on the nature of ultra-microscopic viruses. Bacteriophage 2011, 1, 127–129. [Google Scholar]
- 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, pp. 94–113, Chapter 4. [Google Scholar]
- 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, pp. 415–438, Chapter 16. [Google Scholar]
- Abedon, S.T.; Yin, J. Bacteriophage plaques: Theory and analysis. Meth. Mol. Biol. 2009, 501, 161–174. [Google Scholar]
- 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. [Google Scholar]
- Gallet, R.; Kannoly, S.; Wang, I.N. Effects of bacteriophage traits on plaque formation. BMC Microbiol. 2011, 11, 181. [Google Scholar]
- 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, pp. 37–65, Chapter 2. [Google Scholar]
- Abedon, S.T.; Thomas-Abedon, C. Phage therapy pharmacology. Curr. Pharm. Biotechnol. 2010, 11, 28–47. [Google Scholar]
- Gill, J.J.; Hyman, P. Phage choice, isolation and preparation for phage therapy. Curr. Pharm. Biotechnol. 2010, 11, 2–14. [Google Scholar]
- Lu, T.K.; Collins, J.J. Dispersing biofilms with engineered enzymatic bacteriophage. Proc. Natl. Acad. Sci. U. S. A. 2007, 104, 11197–11202. [Google Scholar]
- Goodridge, L.D. Designing phage therapeutics. Curr. Pharm. Biotechnol. 2010, 11, 15–27. [Google Scholar]
- 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. [Google Scholar]
- 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. [Google Scholar] [CrossRef]
- Abedon, S. Phage therapy pharmacology: Calculating phage dosing. Adv. Appl. Microbiol. 2011, 77, 1–40. [Google Scholar]
- 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. [Google Scholar] [CrossRef]
- Thingstad, T.F.; Bratbak, G.; Heldal, M. Aquatic phage ecology. In Bacteriophage Ecology; Abedon, S.T., Ed.; Cambridge University Press: Cambridge, UK, 2008; pp. 251–280, Chapter 10. [Google Scholar]
- 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. [Google Scholar]
- Schrag, S.; Mittler, J.E. Host-parasite persistence: The role of spatial refuges in stabilizing bacteria-phage interactions. Am. Nat. 1996, 148, 348–377. [Google Scholar]
- Hyman, P.; Abedon, S.T. Bacteriophage host range and bacterial resistance. Adv. Appl. Microbiol. 2010, 70, 217–248. [Google Scholar]
- Labrie, S.J.; Samson, J.E.; Moineau, S. Bacteriophage resistance mechanisms. Nat. Rev. Microbiol. 2010, 8, 317–327. [Google Scholar]
- Abedon, S.T. Bacterial 'immunity' against bacteriophages. Bacteriophage. 2012, 2. Available online: http://www.landesbioscience.com/journals/bacteriophage/article/18609/ (accessed on 13 April 2012).
- Abedon, S.T. Lysis of lysis inhibited bacteriophage T4-infected cells. J. Bacteriol. 1992, 174, 8073–8080. [Google Scholar]
- Abedon, S.T. Envisaging bacteria as phage targets. Bacteriophage 2011, 1, 228–230. [Google Scholar]
- Stent, G.S. Molecular Biology of Bacterial Viruses; WH Freeman and Co.: San Francisco, CA, USA, 1963. [Google Scholar]
- 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. [Google Scholar] [Green Version]
- Abedon, S.T. Phage population growth: Constraints, games, adaptation. In Bacteriophage Ecology; Abedon, S.T., Ed.; Cambridge University Press: Cambridge, UK, 2008; Volume 15, pp. 64–93, Chapter 3. [Google Scholar]
- 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. [Google Scholar]
- Abedon, S.T. Bacteriophage T4 resistance to lysis-inhibition collapse. Genet. Res. 1999, 74, 1–11. [Google Scholar]
- Young, K.D. The selective value of bacterial shape. Microbiol. Mol. Biol. Rev. 2006, 70, 660–703. [Google Scholar]
- Young, K.D. Bacterial morphology: Why have different shapes? Curr. Opin. Microbiol. 2007, 10, 596–600. [Google Scholar]
- Azeredo, J.; Sutherland, I.W. The use of phages for the removal of infectious biofilms. Curr. Pharm. Biotechnol. 2008, 9, 261–266. [Google Scholar]
- Turner, G.F.; Pitcher, T.J. Attack abatement: A model for group protection by combined avoidance and dilution. Am. Nat. 1986, 128, 228–240. [Google Scholar]
- Babic, A.; Berkmen, M.B.; Lee, C.A.; Grossman, A.D. Efficient gene transfer in bacterial cell chains. MBio 2011, 2, e00027-11. [Google Scholar]
- Abedon, S.T. Phages, ecology, evolution. In Bacteriophage Ecology; Abedon, S.T., Ed.; Cambridge University Press: Cambridge, UK, 2008; Volume 15, pp. 1–28, Chapter 1. [Google Scholar]
- Hagens, S.; Loessner, M.J. Bacteriophage for biocontrol of foodborne pathogens: Calculations and considerations. Curr. Pharm. Biotechnol. 2010, 11, 58–68. [Google Scholar]
- Goodridge, L.D. Phages, bacteria, and food. In Bacteriophage Ecology; Abedon, S.T., Ed.; Cambridge University Press: Cambridge, UK, 2008; pp. 302–331, Chapter 12. [Google Scholar]
- Xavier, J.B.; Foster, K.R. Cooperation and conflict in microbial biofilms. Proc. Natl. Acad. Sci. U. S. A. 2007, 104, 876–881. [Google Scholar]
- Wimpenny, J. Ecological determinants of biofilm formation. Biofouling 1996, 10, 43–63. [Google Scholar]
- 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. [Google Scholar]
- Crombach, A.; Hogeweg, P. Evolution of resource cycling in ecosystems and individuals. BMC Evol. Biol. 2009, 9, 122. [Google Scholar]
- Hoffmeister, M.; Martin, W. Interspecific evolution: Microbial symbiosis, endosymbiosis and gene transfer. Environ. Microbiol. 2003, 5, 641–649. [Google Scholar]
- Searcy, D.G. Metabolic integration during the evolutionary origin of mitochondria. Cell Res. 2003, 13, 229–238. [Google Scholar]
- Kreft, J.U. Biofilms promote altruism. Microbiology 2004, 150, 2751–2760. [Google Scholar]
- 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. [Google Scholar]
- Takahashi, N.; Nyvad, B. The role of bacteria in the caries process: Ecological perspectives. J. Dent. Res. 2011, 90, 294–303. [Google Scholar]
- Kolter, R. Biofilms in lab and nature: A molecular geneticist's voyage to microbial ecology. Int. Microbiol. 2010, 13, 1–7. [Google Scholar]
- 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. [Google Scholar]
- 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; pp. 195–213, Chapter11. [Google Scholar]
- 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. [Google Scholar]
- Arciola, C.R. Host defense against implant infection: The ambivalent role of phagocytosis. Int. J. Artif. Organs 2010, 33, 565–567. [Google Scholar]
- Jensen, P.O.; Givskov, M.; Bjarnsholt, T.; Moser, C. The immune system vs. Pseudomonas aeruginosa biofilms. FEMS Immunol. Med. Microbiol. 2010, 59, 292–305. [Google Scholar]
- 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. [Google Scholar]
- 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. [Google Scholar]
- Friend, P.L.; Slade, A.D. Characteristics of group A streptococcal bacteriophages. J. Bacteriol. 1966, 92, 148–154. [Google Scholar]
- 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. [Google Scholar] [CrossRef]
- Kaplan, D.A.; Naumovski, L.; Rothschild, B.; Collier, R.J. Appendix: A model of plaque formation. Gene 1981, 13, 221–225. [Google Scholar]
- 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. [Google Scholar]
- 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; pp. 191–215, Chapter 7. [Google Scholar]
- 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. [Google Scholar]
- 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. [Google Scholar]
- 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. [Google Scholar]
- Abedon, S.T. Phage evolution and ecology. Adv. Appl. Microbiol. 2009, 67, 1–45. [Google Scholar]
- 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. [Google Scholar]
- Abedon, S.T.; Kuhl, S.J.; Blasdel, B.G.; Kutter, E.M. Phage treatment of human infections. Bacteriophage 2011, 1, 66–85. [Google Scholar]
© 2012 by the authors; licensee MDPI, Basel, Switzerland. This article is an open-access article distributed under the terms and conditions of the Creative Commons Attribution license (http://creativecommons.org/licenses/by/3.0/).
Share and Cite
Abedon, S.T. Spatial Vulnerability: Bacterial Arrangements, Microcolonies, and Biofilms as Responses to Low Rather than High Phage Densities. Viruses 2012, 4, 663-687. https://doi.org/10.3390/v4050663
Abedon ST. Spatial Vulnerability: Bacterial Arrangements, Microcolonies, and Biofilms as Responses to Low Rather than High Phage Densities. Viruses. 2012; 4(5):663-687. https://doi.org/10.3390/v4050663
Chicago/Turabian StyleAbedon, Stephen T. 2012. "Spatial Vulnerability: Bacterial Arrangements, Microcolonies, and Biofilms as Responses to Low Rather than High Phage Densities" Viruses 4, no. 5: 663-687. https://doi.org/10.3390/v4050663