Mechanisms of Biofilm Development, Antibiotic Resistance and Tolerance and Their Role in Persistent Infections

Srivastava, Divya; Srivastava, Suchi; Singh, Poonam C.; Kumar, Adesh

doi:10.1007/978-981-13-9871-1_5

Divya Srivastava⁴,
Suchi Srivastava⁵,
Poonam C. Singh⁵ &
…
Adesh Kumar⁴

1006 Accesses

Abstract

Bacteria frequently form biofilms in response to stress factors that include exposure of planktonic cells to subinhibitory concentrations of antibiotics. When these attach to a surface, they switch to the biofilm mode of growth and undergo a phenotypic shift in behaviour. During this process, a large suite of genes are differentially regulated to develop a biofilm, which protect them from killing by antibiotics. This leads to the persistence of biofilm infections and the mechanisms used to protect bacteria in biofilms distinct from those that are responsible for conventional antibiotic resistance as well as tolerance. This tolerance to antibiotics is contributed to by multiple factors such as poor antibiotic penetration, nutrient limitation adaptive stress responses, slowed metabolism and the formation of persister cells. The present chapter deals with the introduction to biofilm and their mechanism to achieve antibiotic resistance as well as tolerance properties including their role in persistent infection with some advancement in biofilm research.

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References

An, D., & Parsek, M. R. (2007). The promise and peril of transcriptional profiling in biofilm communities. Current Opinion in Microbiology, 10(3), 292–296. https://doi.org/10.1016/j.mib.2007.05.011.
Article CAS PubMed Google Scholar
Anderl, J. N., Franklin, M. J., & Stewart, P. S. (2000). Role of antibiotic penetration limitation in Klebsiella pneumoniae biofilm resistance to ampicillin and ciprofloxacin. Antimicrobial Agents and Chemotherapy, 44(7), 1818–1824.
Article CAS PubMed PubMed Central Google Scholar
Anderson, G. G., Dodson, K. W., Hooton, T. M., & Hultgren, S. J. (2004). Intracellular bacterial communities of uropathogenic Escherichia coli in urinary tract pathogenesis. Trends in Microbiology, 12, 424–430. https://doi.org/10.1016/j.tim.2004.07.005.
Article CAS PubMed Google Scholar
Ashby, M. J., Neale, J. E., Knott, S. J., & Critchley, I. A. (1994). Effect of antibiotics on non-growing planktonic cells and biofilms of Escherichia coli. Journal of Antimicrobial Chemotherapy, 33(3), 443–452. https://doi.org/10.1093/jac/33.3.443.
Article CAS PubMed Google Scholar
Aslam, S. N., Cresswell-Maynard, T., Thomas, D. N., & Underwood, G. J. (2012). Production and characterization of the intra-and extracellular carbohydrates and polymeric substances (EPS) of three sea-ice diatom species, and evidence for a cryoprotective role for EPS. Journal of Phycology, 48(6), 1494–1509. https://doi.org/10.1111/jpy.12004.
Article CAS PubMed Google Scholar
Balaban, N. Q., Merrin, J., Chait, R., Kowalik, L., & Leibler, S. (2004). Bacterial persistence as a phenotypic switch. Science, 305, 1622–1625. https://doi.org/10.1126/science.1099390.
Article CAS PubMed Google Scholar
Baselga, R., Albizu, I., & Amorena, B. (1994). Staphylococcus aureus capsule and slime as virulence factors in ruminant mastitis. A review. Veterinary Microbiology, 39, 195–204. https://doi.org/10.1016/0378-1135(94)90157-0.
Article CAS PubMed Google Scholar
Borriello, G., Werner, E., Roe, F., Kim, A. M., Ehrlich, G. D., & Stewart, P. S. (2004). Oxygen limitation contributes to antibiotic tolerance of Pseudomonas aeruginosa in biofilms. Antimicrobial Agents and Chemotherapy, 48(7), 2659–2664. https://doi.org/10.1128/AAC.48.7.2659-2664.2004.
Article CAS PubMed PubMed Central Google Scholar
Branda, S. S., Chu, F., Kearns, D. B., Losick, R., & Kolter, R. (2006). A major protein component of the Bacillus subtilis biofilm matrix. Molecular Microbiology, 59(4), 1229–1238. https://doi.org/10.1111/j.1365-2958.2005.05020.x.
Article CAS PubMed Google Scholar
Carl, V. C., Graham, J. C., Underwood, J. S., & David, M. P. (2014). Ecology of intertidal microbial biofilms: Mechanisms, patterns and future research needs. Journal of Sea Research, 92, 2–5. https://doi.org/10.1016/j.seares.2014.07.003.
Article Google Scholar
Chakraborty, S., Dutta, T. K., De, A., Das, M., & Ghosh, S. (2018). Impact of bacterial biofilm in veterinary medicine: An overview. International Journal of Current Microbiology and Applied Sciences, 7(04), 3228–3239. https://doi.org/10.20546/ijcmas.2018.704.366.
Article CAS Google Scholar
Chiang, W. C., Nilsson, M., Jensen, P. Ø., Høiby, N., Nielsen, T. E., Givskov, M., & Tolker-Nielsen, T. (2013). Extracellular DNA shields against aminoglycosides in Pseudomonas aeruginosa biofilms. Antimicrobial Agents and Chemotherapy, 57(5), 2352–2361. https://doi.org/10.1128/AAC.00001-13. Epub 2013 Mar 11.
Article CAS PubMed PubMed Central Google Scholar
Chimileski, S., Franklin, M. J., & Papke, R. T. (2014). Biofilms formed by the archaeon Haloferax volcanii exhibit cellular differentiation and social motility, and facilitate horizontal gene transfer. BMC Biology, 12, 65. https://doi.org/10.1186/s12915-014-0065-5.
Article CAS PubMed PubMed Central Google Scholar
Ciofu, O., Tolker-Nielsen, T., Jensen, P. Ø., Wang, H., & Høiby, N. (2014). Antimicrobial resistance, respiratory tract infections and role of biofilms in lung infections in cystic fibrosis patients. Advanced Drug Delivery Reviews, 85, 7–23. https://doi.org/10.1016/j.addr.2014.11.017. Epub 2014 Dec 2.
Article CAS PubMed Google Scholar
Costerone, J. W., Stewart, P. S., & Greenberg, E. P. (1999). Bacterial biofilms: A common cause of persistent infections. Science, 284, 1318–1322. https://doi.org/10.1126/science.284.5418.1318.
Article Google Scholar
Costerton, J. W., Lewandowski, Z., Caldwell, D. E., Korber, D. R., & Lappin-Scott, H. M. (1995). Microbial biofilms. Annual Review of Microbiology, 49(1), 711–745. https://doi.org/10.1146/annurev.mi.49.100195.003431.
Article CAS PubMed Google Scholar
Costerton, J. W., Veeh, R., & Shirtliff, M. (2003). The application of biofilm science to the study and control of chronic bacterial infections. Journal of Clinical Investigation, 112, 1466–1477. https://doi.org/10.1172/JCI20365.
Article CAS PubMed PubMed Central Google Scholar
Danhorn, T., & Fuqua, C. (2007). Biofilm formation by plant-associated bacteria. Annual Review of Microbiology, 61, 401–422. https://doi.org/10.1146/annurev.micro.61.080706.093316.
Article CAS PubMed Google Scholar
de Beer, D., Stoodley, P., & Lewandowski, Z. (1997). Measurement of local diffusion coefficients in biofilms by microinjection and confocal microscopy. Biotechnology and Bioengineering, 53(2), 151–158. https://doi.org/10.1002/(SICI)1097-0290(19970120)53:2<151::AID-BIT4>3.0.CO;2-N.
Article PubMed Google Scholar
Donlan, R. M., & Costerton, J. W. (2002). Biofilms survival mechanisms of clinically relevant microorganisms. Clinical Microbiology Reviews, 15, 167–193. https://doi.org/10.1128/CMR.15.2.167-193.2002.
Article CAS PubMed PubMed Central Google Scholar
Fux, C. A., Wilson, S., & Stoodley, P. (2004). Detachment characteristics and oxacillin resistance of Staphyloccocus aureus biofilm emboli in an in vitro catheter infection model. Journal of Bacteriology, 186(14), 4486–4491. https://doi.org/10.1128/JB.186.14.4486-4491.2004.
Article CAS PubMed PubMed Central Google Scholar
Hall-Stoodley, L., & Stoodley, P. (2009). Evolving concepts in biofilm infections. Cellular Microbiology, 11(7), 1034–1043. https://doi.org/10.1111/j.1462-5822.2009.01323.x. Epub 2009 Apr 6.
Article CAS PubMed Google Scholar
Hall-Stoodley, L., Costerton, J. W., & Stoodley, P. (2004). Bacterial biofilms: From the natural environment to infectious diseases. Nature Reviews Microbiology, 2(2), 95–108. https://doi.org/10.1038/nrmicro821.
Article CAS PubMed Google Scholar
Hoffman, L. R., D’Argenio, D. A., MacCoss, M. J., Zhang, Z., Jones, R. A., & Miller, S. I. (2005). Aminoglycoside antibiotics induce bacterial biofilm formation. Nature, 436(7054), 1171–1175. https://doi.org/10.1038/nature03912.
Article CAS PubMed Google Scholar
Hu, Y., & Coates, A. (2012). Nonmultiplying bacteria are profoundly tolerant to antibiotics. In A. R. M. Coates (Ed.), Antibiotic resistance (Handbook of experimental pharmacology) (Vol. 211, pp. 99–119). Berlin Heidelberg: Springer. https://doi.org/10.1007/978-3-642-28951-4-7.
Chapter Google Scholar
Jakubovics, N. S., Shields, R. C., Rajarajan, N., & Burgess, J. G. (2013). Life after death: The critical role of extracellular DNA in microbial biofilms. Letters in Applied Microbiology, 57(6), 467–475. https://doi.org/10.1111/lam.12134.
Article CAS PubMed Google Scholar
Jolivet-Gougeon, A., & Bonnaure-Mallet, M. (2014). Biofilms as a mechanism of bacterial resistance. Drug Discovery Today: Technologies, 11, 49–56. https://doi.org/10.1016/j.ddtec.2014.02.003.
Article PubMed Google Scholar
Joubert, L. M., Wolfaardt, G. M., & Botha, A. (2006). Microbial exopolymers link predator and prey in a model yeast biofilm system. Microbial Ecology, 52(2), 187–197. https://doi.org/10.1007/s00248-006-9063-7.
Article PubMed Google Scholar
Karthik, R., Ambica, R., & Nagarathnamma, T. (2018). Study of biofilm production and antimicrobial susceptibility pattern in clinical isolates of proteus species at a tertiary care hospital. International Journal of Current Microbiology and Applied Sciences, 7(01), 574–586. https://doi.org/10.20546/ijcmas.2018.701.070.
Article CAS Google Scholar
Keren, I., Shah, D., Spoering, A., Kaldalu, N., & Lewis, K. (2004). Specialized persister cells and the mechanism of multidrug tolerance in Escherichia coli. Journal of Bacteriology, 186(24), 8172–8180. https://doi.org/10.1128/JB.186.24.8172-8180.2004.
Article CAS PubMed PubMed Central Google Scholar
Kindrachuk, J., Scruten, E., Attah-Poku, S., Bell, K., Potter, A., Babiuk, L. A., Griebel, P. J., & Napper, S. (2011). Stability, toxicity, and biological activity of host defense peptide BMAP28 and its inversed and retro-inversed isomers. Biopolymers, 96(1), 14–24. https://doi.org/10.1002/bip.21441.
Article CAS PubMed Google Scholar
Lazăr, V., & Chifiriuc, M. C. (2010). Medical significance and new therapeutical strategies for biofilm associated infections. Romanian Archives of Microbiology and Immunology, 69(3), 125–138. on www.researchgate.net/publication/50849066.
PubMed Google Scholar
Leid, J. G., Willson, C. J., Shirtliff, M. E., Hassett, D. J., Parsek, M. R., & Jeffers, A. K. (2005). The exopolysaccharide alginate protects Pseudomonas aeruginosa biofilm bacteria from IFNgamma- mediated macrophage killing. Journal of Immunology, 175(11), 7512–7518. https://doi.org/10.4049/jimmunol.175.11.7512.
Article CAS Google Scholar
Lenz, A. P., Williamson, K. S., Pitts, B., Stewart, P. S., & Franklin, M. J. (2008). Localized gene expression in Pseudomonas aeruginosa biofilms. Applied and Environmental Microbiology, 74(14), 4463–4471. https://doi.org/10.1128/AEM.00710-08. Epub 2008 May 16.
Article CAS PubMed PubMed Central Google Scholar
Lewis, K. (2007). Persister cells, dormancy and infectious disease. Nature Reviews Microbiology, 5(1), 48–56. https://doi.org/10.1038/nrmicro1557.
Article CAS PubMed Google Scholar
Lewis, K. (2012). Persister cells: molecular mechanisms related to antibiotic tolerance. In A. R. M. Coates (Ed.), Antibiotic resistance (Handbook of experimental pharmacology) (Vol. 211, pp. 121–133). Berlin Heidelberg: Springer. https://doi.org/10.1007/978-3-642-28951-4_8.
Chapter Google Scholar
Luppens, S. B., Reij, M. W., van der Heijden, R. W., Rombouts, F. M., & Abee, T. (2002). Development of a standard test to assess the resistance of Staphylococcus aureus biofilm cells to disinfectants. Applied and Environmental Microbiology, 68(9), 4194–4200. https://doi.org/10.1128/AEM.68.9.4194-4200.2002.
Article CAS PubMed PubMed Central Google Scholar
Mckenney, D. (1998). The ica locus of Staphylococcus epidermidis encodes production of the capsular polysaccharide/adhesin. Infect Immunity, 66, 4711–4720.
CAS Google Scholar
Molin, S., & Tolker-Nielsen, T. (2003). Gene transfer occurs with enhanced efficiency in biofilms and induces enhanced stabilisation of the biofilm structure. Current Opinion in Biotechnology, 14(3), 255–261. https://doi.org/10.1016/S0958-1669(03)00036-3.
Article CAS PubMed Google Scholar
Monroe, D. (2007). Looking for chinks in the armor of bacterial biofilms. PLoS Biology, 5(11). https://doi.org/10.1371/journal.pbio.0050307.
Article PubMed PubMed Central Google Scholar
Muhsin, J., Ahmad, W., Andleeb, S., Jalil, F., Nawaz, M. A., Hussain, T., Muhammad, A., Muhammad, R., & Muhammad, A. K. (2018). Bacterial biofilm and associated infections. Journal of the Chinese Medical Association, 81(1), 7–11. https://doi.org/10.1016/j.jcma.2017.07.012.
Article Google Scholar
Nadell, C. D., Xavier, J. B., & Foster, K. R. (2009). The sociobiology of biofilms. FEMS Microbiology Reviews, 33(1), 206–224. https://doi.org/10.1111/j.1574-6976.2008.00150.x.
Article CAS PubMed Google Scholar
Nickel, J. C., Ruseska, I., Wright, J. B., & Costerton, J. W. (1985). Tobramycin resistance of Pseudomonas aeruginosa cells growing as a biofilm on urinary catheter material. Antimicrobial Agents and Chemotherapy, 27(4), 619–624. https://doi.org/10.1128/AAC.27.4.619.
Article CAS PubMed PubMed Central Google Scholar
O’Toole, G. A., & Kolter, R. (May 1998). Initiation of biofilm formation in Pseudomonas fluorescens WCS365 proceeds via multiple, convergent signalling pathways: A genetic analysis. Molecular Microbiology, 28(3), 449–461. https://doi.org/10.1046/j.1365-2958.1998.00797.x.
Article PubMed Google Scholar
Ojha, A. K., Baughn, A. D., & Sambandan, D. (2008). Growth of Mycobacterium tuberculosis biofilms containing free mycolic acids and harbouring drug-tolerant bacteria. Molecular Microbiology, 69, 164–174. https://doi.org/10.1111/j.1365-2958.2008.06274.x.
Article CAS PubMed PubMed Central Google Scholar
Pamp, S. J., Gjermansen, M., Johansen, H. K., & Tolker-Nielsen, T. (2008). Tolerance to the antimicrobial peptide colistin in Pseudomonas aeruginosa biofilms is linked to metabolically active cells, and depends on the pmr and mexAB-oprM genes. Molecular Microbiology, 68(1), 223–240. https://doi.org/10.1111/j.1365-2958.2008.06152.x. Epub 2008 Feb 28.
Article CAS PubMed Google Scholar
Paramasivam, N., Pandian, S. K., Kushmaro, A., Voravuthi kunchai, S., & Wilson, A. (2017). Recent advances in biofilmology and antibiofilm measures. BioMed Research International, 5409325. https://doi.org/10.1155/2017/5409325.
Article Google Scholar
Parsek, M. R., & Singh, P. K. (2003). Bacterial biofilms: An emerging link to disease pathogenesis. Annual Review of Microbiology, 57, 677–701. https://doi.org/10.1146/annurev.micro.57.030502.090720.
Article CAS PubMed Google Scholar
Römling, U., & Balsalobre, C. (2012). Biofilm infections, their resilience to therapy and innovative treatment strategies. Journal of Internal Medicine, 272(6), 541–561. https://doi.org/10.1111/joim.12004. Epub 2012 Oct 29.
Article CAS PubMed Google Scholar
Savage, V. J., Chopra, I., & O’Neill, A. J. (2013). Staphylococcus aureus biofilms promote horizontal transfer of antibiotic resistance. Antimicrobial Agents and Chemotherapy, 57(4), 1968–1970. https://doi.org/10.1128/AAC.02008-12.
Article CAS PubMed PubMed Central Google Scholar
Schaible, B., Taylor, C. T., & Schaffer, K. (2012). Hypoxia increases antibiotic resistance in Pseudomonas aeruginosa through altering the composition of multidrug efflux pumps. Antimicrobial Agents and Chemotherapy, 56(4), 2114–2118. https://doi.org/10.1128/AAC.05574-11.
Article CAS PubMed PubMed Central Google Scholar
Singh, P. K., Schaefer, A. L., & Parsek, M. R. (2000). Quorum-sensing signals indicate that cystic fibrosis lungs are infected with bacterial biofilms. Nature, 407, 762–764. https://doi.org/10.1038/35037627.
Article CAS PubMed Google Scholar
Spoering, A. L., & Lewis, K. (2001). Biofilms and planktonic cells of Pseudomonas aeruginosa have similar resistance to killing by antimicrobials. Journal of Bacteriology, 183(23), 6746–6751. https://doi.org/10.1128/JB.183.23.6746-6751.2001.
Article CAS PubMed PubMed Central Google Scholar
Stewart, P. S., & Costerton, J. W. (2001). Antibiotic resistance of bacteria in biofilms. Lancet, 358(9276), 135–138. https://doi.org/10.1016/S0140-6736(01)05321-1.
Article CAS PubMed Google Scholar
Stoodley, P., deBeer, D., & Zbigniew, L. (1994). Liquid flow in biofilm systems. Applied and Environmental Microbiology, 60(8), 2711–2716.
CAS PubMed PubMed Central Google Scholar
Suci, P. A., Mittelman, M. W., Yu, F. P., & Geesey, G. G. (1994). Investigation of ciprofloxacin penetration into Pseudomonas aeruginosa biofilms. Antimicrobial Agents and Chemotherapy, 38(9), 2125–2133. https://doi.org/10.1128/AAC.38.9.2125.
Article CAS PubMed PubMed Central Google Scholar
Taylor, P. K., Yeung, A. T., & Hancock, R. E. (2014). Antibiotic resistance in Pseudomonas aeruginosa biofilms: Towards the development of novel anti-biofilm therapies. Journal of Biotechnology, 191, 121–130. https://doi.org/10.1016/j.jbiotec.2014.09.003. Epub 2014 Sep 18.
Article CAS PubMed Google Scholar
Vert, M., Doi, Y., Hellwich, K. H., Hess, M., Hodge, P., Kubisa, P., Rinaudo, M., & Schué, F. (2012). Terminology for biorelated polymers and applications (IUPAC Recommendations 2012). Pure and Applied Chemistry, 84(2), 377–410. https://doi.org/10.1351/PAC-REC-10-12-04.
Article CAS Google Scholar
Vlamakis, H., Aguilar, C., Losick, R., & Kolter, R. (2008). Control of cell fate by the formation of an architecturally complex bacterial community. Genes & Development, 22(7), 945–953. https://doi.org/10.1101/gad.1645008.
Article CAS Google Scholar
Walters, M. C., Roe, F., Bugnicourt, A., Franklin, M. J., & Stewart, P. S. (2003). Contributions of antibiotic penetration, oxygen limitation, and low metabolic activity to tolerance of Pseudomonas aeruginosa biofilms to ciprofloxacin and tobramycin. Antimicrobial Agents and Chemotherapy, 47(1), 317–323. https://doi.org/10.1128/AAC.47.1.317-323.2003.
Article CAS PubMed PubMed Central Google Scholar
Werner, E., Roe, F., Bugnicourt, A., Franklin, M. J., Heydorn, A., Molin, S., Pitts, B., & Stewart, P. S. (2004). Stratified growth in Pseudomonas aeruginosa biofilms. Applied and Environmental Microbiology, 70(10), 6188–6196. https://doi.org/10.1128/AEM.70.10.6188-6196.2004.
Article CAS PubMed PubMed Central Google Scholar
Wingender, J., & Flemming, H. C. (2010). The biofilm matrix. Nature Reviews Microbiology, 8, 623–633. https://doi.org/10.1038/nrmicro2415.
Article CAS PubMed Google Scholar
Xu, K. D., McFeters, G. A., & Stewart, P. S. (2000). Biofilm resistance to antimicrobial agents. Microbiology, 146(Pt 3), 547–549. https://doi.org/10.1099/00221287-146-3-547.
Article CAS PubMed Google Scholar
Zhang, L., & Mah, T. F. (2008). Involvement of a novel efflux system in biofilm-specific resistance to antibiotics. Journal of Bacteriology, 190(13), 4447–4452. https://doi.org/10.1128/JB.01655-07.
Article CAS PubMed PubMed Central Google Scholar

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Narendra Deva University of Agriculture and Technology, Faizabad, Uttar Pradesh, India
Divya Srivastava & Adesh Kumar
CSIR- National Botanical Research Institute, Lucknow, Uttar Pradesh, India
Suchi Srivastava & Poonam C. Singh

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Divya Srivastava
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Suchi Srivastava
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Poonam C. Singh
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Adesh Kumar
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Agricultural Microbiology, Faculty of Agricultural Sciences, Aligarh Muslim University, Aligarh, Uttar Pradesh, India
Iqbal Ahmad
Institute of Ophthalmology, JN Medical College, Aligarh Muslim University, Aligarh, Uttar Pradesh, India
Shamim Ahmad
School of Medicine, Texas Tech University Health Sciences Center, Lubbock, TX, USA
Kendra P. Rumbaugh

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Srivastava, D., Srivastava, S., Singh, P.C., Kumar, A. (2019). Mechanisms of Biofilm Development, Antibiotic Resistance and Tolerance and Their Role in Persistent Infections. In: Ahmad, I., Ahmad, S., Rumbaugh, K. (eds) Antibacterial Drug Discovery to Combat MDR. Springer, Singapore. https://doi.org/10.1007/978-981-13-9871-1_5

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DOI: https://doi.org/10.1007/978-981-13-9871-1_5
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