Bacterial exo-polysaccharides in biofilms: role in antimicrobial resistance and treatments
Tóm tắt
Bacterial biofilms are aggregation or collection of different bacterial cells which are covered by self-produced extracellular matrix and are attached to a substratum. Generally, under stress or in unfavorable conditions, free planktonic bacteria transform themselves into bacterial biofilms and become sessile. Various mechanisms involving interaction between antimicrobial and biofilm matrix components, reduced growth rates, and genes conferring antibiotic resistance have been described to contribute to enhanced resistance. Quorum sensing and multi-drug resistance efflux pumps are known to regulate the internal environment within the biofilm as well as biofilm formation; they also protect cells from antibiotic attack or immune attacks. This review summarizes data supporting the importance of exopolysaccharides during biofilm formation and its role in antibiotic resistance. Involvement of quorum sensing and efflux pumps in antibiotic resistance in association with exopolysaccharides. Also, strategies to overcome or attack biofilms are provided.
Tài liệu tham khảo
Sharma D, Misba L, Khan AU (2019) Antibiotics versus biofilm: an emerging battleground in microbial communities. Antimicrob Resist Infect Control 8(1):1–10. https://doi.org/10.1186/s13756-019-0533-3
Gupta P, Pruthi PA, Pruthi V (2019) Role of exopolysaccharides in biofilm formation. In: Introduction to biofilm engineering. American Chemical Society, pp 17–57. https://doi.org/10.1021/bk-2019-1323.ch002
Soto SM (2013) Role of efflux pumps in the antibiotic resistance of bacteria embedded in a biofilm. Virulence 4(3):223–229. https://doi.org/10.4161/viru.23724
Van Acker H, Coenye T (2016) The role of efflux and physiological adaptation in biofilm tolerance and resistance. J Biol Chemist 291(24):12565–12572. https://doi.org/10.1074/jbc.R115.707257
Chandki R, Banthia P, Banthia R (2011) Biofilms: a microbial home. J Indian Soc Periodontol 15(2):111. https://doi.org/10.4103/0972-124X.84377
Yasir M, Willcox MDP, Dutta D (2018) Action of antimicrobial peptides against bacterial biofilms. Materials 11(12):2468. https://doi.org/10.3390/ma11122468
Nwodo UU, Green E, Okoh AI (2012) Bacterial exopolysaccharides: functionality and prospects. Int J mol sci 13(11):14002–14015. https://doi.org/10.3390/ijms131114002
Miller MB, Bassler BL (2001) Quorum sensing in bacteria. Annu Rev Microbiol 55(1):165–199. https://doi.org/10.1146/annurev.micro.55.1.165
Yan J, Bassler BL (2019) Surviving as a community: antibiotic tolerance and persistence in bacterial biofilms. Cell Host & Microbe 26(1):15–21. https://doi.org/10.1016/j.chom.2019.06.002
Bassler, B. L. (1999). How bacteria talk to each other: regulation of gene expression by quorum sensing. Curr Opin in Microbiol, 2(6), 582-587. https://doi.org/10.1016/S1369-5274(99)00025-9
Watanabe K, Tabuchi M, Morinaga Y, Yoshinaga F (1998) Structural features and properties of bacterial cellulose produced in agitated culture. Cellulose 5(3):187–200. https://doi.org/10.1023/A:1009272904582
Karygianni L, Ren Z, Koo H, Thurnheer T (2020) Biofilm matrixome: extracellular components in structured microbial communities. Trends in Microbiol 28(8):668–681. https://doi.org/10.1016/j.tim
Limoli DH, Jones CJ, Wozniak DJ (2015) Bacterial extracellular polysaccharides in biofilm formation and function. Microbiol spectrum 3(3). https://doi.org/10.1128/microbiolspec.MB-0011-2014
Maunders E, Welch M (2017) Matrix exopolysaccharides; the sticky side of biofilm formation. FEMS Microbiol Letters 364(13):fnx120. https://doi.org/10.1093/femsle/fnx120
Liu J, Zhang J, Guo L, Zhao W, Hu X, Wei X (2017) Inactivation of a putative efflux pump (LmrB) in Streptococcus mutans results in altered biofilm structure and increased exopolysaccharide synthesis: implications for biofilm resistance. Biofouling 33(6):481–493. https://doi.org/10.1080/08927014.2017.1323206
Saxena P, Joshi Y, Rawat K, Bisht R (2019) Biofilms: architecture, resistance, quorum sensing and control mechanisms. Indian J microbiol 59(1):3–12. https://doi.org/10.1007/s12088-018-0757-6
Kostakioti M, Hadjifrangiskou M, Hultgren SJ (2013) Bacterial biofilms: development, dispersal, and therapeutic strategies in the dawn of the postantibiotic era. Cold Spring Harbor Perspectives in Med 3(4):a010306. https://doi.org/10.1101/cshperspect.a010306
Alav I, Sutton JM, Rahman KM (2018) Role of bacterial efflux pumps in biofilm formation. J Antimicrob Chemotherapy 73(8):2003–2020. https://doi.org/10.1093/jac/dky042
Geske GD, Wezeman RJ, Siegel AP, Blackwell HE (2005) Small molecule inhibitors of bacterial quorum sensing and biofilm formation. J Am Chem Soc 127(37):12762–12763. https://doi.org/10.1021/ja0530321
Martins M, McCusker M, Amaral L, Fanning S (2011) Mechanisms of antibiotic resistance in Salmonella: efflux pumps, genetics, quorum sensing and biofilm formation. Letters in Drug Design & Discovery 8(2):114–123. https://doi.org/10.2174/157018011794183770
Lembre, Pierre, Cécile Lorentz, and Patrick Di Martino. "Exopolysaccharides of the biofilm matrix: a complex biophysical world." The complex world of polysaccharides (2012): 371-392.
Zavilgelsky GB, Manukhov IV (2001) Quorum sensing, or how bacteria “talk” to each other. Mol Biol 35(2):224–232. https://doi.org/10.1023/A:1010439501530
Papenfort K, Bassler BL (2016) Quorum sensing signal–response systems in Gram-negative bacteria. Nat Rev Microbiol 14(9):576–588. https://doi.org/10.1038/nrmicro.2016.89
Prüß BM (2017) Involvement of two-component signaling on bacterial motility and biofilm development. Journal of bacteriology 199(18). https://doi.org/10.1128/JB.00259-17
Schilcher K, Horswill AR (2020) Staphylococcal biofilm development: structure, regulation, and treatment strategies. Microbiol and Mol Biol Rev 84(3). https://doi.org/10.1128/MMBR.00026-19
O'Toole GA, Kolter R (1998) Flagellar and twitching motility are necessary for Pseudomonas aeruginosa biofilm development. Mol microbiol 30(2):295–304. https://doi.org/10.1046/j.1365-2958.1998.01062.x
Webber MA, Piddock LJV (2003) The importance of efflux pumps in bacterial antibiotic resistance. J antimicrob chemotherapy 51(1):9–11. https://doi.org/10.1093/jac/dkg050
Sun J, Deng Z, Yan A (2014) Bacterial multidrug efflux pumps: mechanisms, physiology and pharmacological exploitations. Biochemical and Biophysical Research Communications 453(2):254–267. https://doi.org/10.1016/j.bbrc.2014.05.090
Du D, Wang-Kan X, Neuberger A, van Veen HW, Pos KM, Piddock LJ, Luisi BF (2018) Multidrug efflux pumps: structure, function and regulation. Nat Rev Microbiol 16(9):523–539. https://doi.org/10.1038/s41579-018-0048-6
Al Rashed N, Joji RM, Saeed NK, Bindayna KM (2020) Detection of overexpression of efflux pump expression in fluoroquinolone-resistant Pseudomonas aeruginosa isolates. Int J App and Basic Med Res 10(1):37–42. https://doi.org/10.4103/ijabmr.IJABMR_90_19
Martinez JL, Sánchez MB, Martínez-Solano L, Hernandez A, Garmendia L, Fajardo A, Alvarez-Ortega C (2009) Functional role of bacterial multidrug efflux pumps in microbial natural ecosystems. FEMS microbiology reviews 33(2):430–449. https://doi.org/10.1111/j.1574-6976.2008.00157.x
Murugan K, Selvanayaki K, Al-Sohaibani S (2016) Urinary catheter indwelling clinical pathogen biofilm formation, exopolysaccharide characterization and their growth influencing parameters. Saudi journal of biological sciences 23(1):150–159. https://doi.org/10.1016/j.sjbs.2015.04.016
Periasamy S, Nair HAS, Lee KWK, Ong J, Goh JQJ, Kjelleberg S, Rice SA (2015) Pseudomonas aeruginosa PAO1 exopolysaccharides are important for mixed species biofilm community development and stress tolerance. Frontiers in microbiology 6:851. https://doi.org/10.3389/fmicb.2015.00851
Vasudevan, S., Joseph, H. A., Swamy, S. S., & Solomon, A. P. (2019). Antibiotic resistance in biofilms. In Introduction to Biofilm Engineering (pp. 205-224). American Chemical Society.
Ciofu O, Tolker-Nielsen T (2019) Tolerance and resistance of Pseudomonas aeruginosa biofilms to antimicrobial agents—how P. aeruginosa can escape antibiotics. Frontiers in microbiology 10:913. https://doi.org/10.3389/fmicb.2019.00913
Hathroubi S, Mekni MA, Domenico P, Nguyen D, Jacques M (2017) Biofilms: microbial shelters against antibiotics. Microbial Drug Resistance 23(2):147–156. https://doi.org/10.1089/mdr.2016.0087
Bowler P, Murphy C, Wolcott R (2020) Biofilm exacerbates antibiotic resistance: Is this a current oversight in antimicrobial stewardship? Antimicrobial Resistance & Infection Control 9(1):1–5. https://doi.org/10.1186/s13756-020-00830-6
Lewis K (2001) Riddle of biofilm resistance. Antimicrobial Agents and Chemotherapy 45(4):999–1007. https://doi.org/10.1128/AAC.45.4.999-1007.2001
Stewart PS (2015) Antimicrobial tolerance in biofilms. Microbial biofilms:269–285. https://doi.org/10.1128/9781555817466.ch13
Billings N, Millan MR, Caldara M, Rusconi R, Tarasova Y, Stocker R, Ribbeck K (2013) The extracellular matrix component Psl provides fast-acting antibiotic defense in Pseudomonas aeruginosa biofilms. PLoS Pathog 9(8):e1003526. https://doi.org/10.1371/journal.ppat.1003526
Colvin KM, Gordon VD, Murakami K, Borlee BR, Wozniak DJ, Wong GC, Parsek MR (2011) The pel polysaccharide can serve a structural and protective role in the biofilm matrix of Pseudomonas aeruginosa. PLoS Pathog 7(1):e1001264. https://doi.org/10.1371/journal.ppat.1001264
Baker P, Hill PJ, Snarr BD, Alnabelseya N, Pestrak MJ, Lee MJ, Jennings LK et al (2016) Exopolysaccharide biosynthetic glycoside hydrolases can be utilized to disrupt and prevent Pseudomonas aeruginosa biofilms. Science Advances 2(5):e1501632. https://doi.org/10.1126/sciadv.1501632
van Tilburg Bernardes E, Charron-Mazenod L, Reading DJ, Reckseidler-Zenteno SL, Lewenza S (2017) Exopolysaccharide-repressing small molecules with antibiofilm and antivirulence activity against Pseudomonas aeruginosa. Antimicrobial Agents and Chemotherapy 61(5). https://doi.org/10.1128/AAC.01997-16
Emami S, Nikokar I, Ghasemi Y, Ebrahimpour M, Ebrahim-Saraie HS, Araghian A, Faezi S, Farahbakhsh M, Rajabi A (2015) Antibiotic resistance pattern and distribution of pslA gene among biofilm producing Pseudomonas aeruginosa isolated from waste water of a burn center. Jundishapur journal of microbiology 8:11. https://doi.org/10.5812/jjm.23669
Begun J, Gaiani JM, Rohde H, Mack D, Calderwood SB, Ausubel FM, Sifri CD (2007) Staphylococcal biofilm exopolysaccharide protects against Caenorhabditis elegans immune defenses. PLoS Pathog 3(4):e57. https://doi.org/10.1371/journal.ppat.0030057
Mishra M, Byrd MS, Sergeant S, Azad AK, Parsek MR, McPhail L, Schlesinger LS, Wozniak DJ (2012) Pseudomonas aeruginosa Psl polysaccharide reduces neutrophil phagocytosis and the oxidative response by limiting complement-mediated opsonization. Cellular microbiology 14(1):95–106. https://doi.org/10.1111/j.1462-5822.2011.01704.x
Leid JG, Willson CJ, Shirtliff ME, Hassett DJ, Parsek MR, Jeffers AK (2005) The exopolysaccharide alginate protects Pseudomonas aeruginosa biofilm bacteria from IFN-γ-mediated macrophage killing. The Journal of Immunology 175(11):7512–7518. https://doi.org/10.4049/jimmunol.175.11.7512
Goltermann L, Tolker-Nielsen T (2017) Importance of the exopolysaccharide matrix in antimicrobial tolerance of Pseudomonas aeruginosa aggregates. Antimicrobial Agents and Chemotherapy 61(4). https://doi.org/10.1128/AAC.02696-16
Muñoz VL, Porsch EA, St. Geme III JW (2018) Kingella kingae surface polysaccharides promote resistance to human serum and virulence in a juvenile rat model. Infect Immun 86(6):e00100-18. https://doi.org/10.1128/IAI.00100-18
Vazquez-Rodriguez A, Vasto-Anzaldo XG, Perez DB, Vázquez-Garza E, Chapoy-Villanueva H, García-Rivas G et al (2018) Microbial competition of Rhodotorula mucilaginosa UANL-001L and E. coli increase biosynthesis of non-toxic exopolysaccharide with applications as a wide-spectrum antimicrobial. Scientific Reports 8(1):1–14. https://doi.org/10.1038/s41598-017-17908-8
Cunha MV, Sousa SA, Leitão JH, Moreira LM, Videira PA, Sá-Correia I (2004) Studies on the involvement of the exopolysaccharide produced by cystic fibrosis-associated isolates of the Burkholderia cepacia complex in biofilm formation and in persistence of respiratory infections. Journal of clinical microbiology 42(7):3052–3058. https://doi.org/10.1128/JCM.42.7.3052-3058.2004
Trivedi A, Mavi PS, Bhatt D, Kumar A (2016) Thiol reductive stress induces cellulose-anchored biofilm formation in Mycobacterium tuberculosis. Nature communications 7(1):1–15. https://doi.org/10.1038/ncomms11392
Perez AC, Pang B, King LB, Tan L, Murrah KA, Reimche JL, Wren JT, Richardson SH, Ghandi U, Swords WE (2014) Residence of Streptococcus pneumoniae and Moraxella catarrhalis within polymicrobial biofilm promotes antibiotic resistance and bacterial persistence in vivo. Pathogens and Disease 70(3):280–288. https://doi.org/10.1111/2049-632X.12129
Kim D, Liu Y, Benhamou RI, Sanchez H, Simón-Soro Á, Li Y, Hwang G, Fridman M, Andes DR, Koo H (2018) Bacterial-derived exopolysaccharides enhance antifungal drug tolerance in a cross-kingdom oral biofilm. The ISME Journal 12(6):1427–1442. https://doi.org/10.1038/s41396-018-0113-1
Ostapska H, Howell PL, Sheppard DC (2018) Deacetylated microbial biofilm exopolysaccharides: it pays to be positive. PLoS pathogens 14(12):e1007411. https://doi.org/10.1371/journal.ppat.1007411
Otto M (2006) Bacterial evasion of antimicrobial peptides by biofilm formation. Antimicrobial Peptides and Human Disease:251–258. https://doi.org/10.1007/3-540-29916-5_10
Mao Y, Doyle MP, Chen J (2006) Role of colanic acid exopolysaccharide in the survival of enterohaemorrhagic Escherichia coli O157: H7 in simulated gastrointestinal fluids. Letters in Applied Microbiology 42(6):642–647. https://doi.org/10.1111/j.1472-765X.2006.01875.x
Ishida T, Ikeda T, Takiguchi N, Kuroda A, Ohtake H, Kato J (2007) Inhibition of quorum sensing in Pseudomonas aeruginosa by N-acyl cyclopentylamides. Applied and Environmental Microbiology 73(10):3183–3188. https://doi.org/10.1128/AEM.02233-06
Sakuragi Y, Kolter R (2007) Quorum-sensing regulation of the biofilm matrix genes (pel) of Pseudomonas aeruginosa. Journal of Bacteriology 189(14):5383–5386. https://doi.org/10.1128/JB.00137-07
Kırmusaoğlu S (2016) Staphylococcal biofilms: pathogenicity, mechanism and regulation of biofilm formation by quorum sensing system and antibiotic resistance mechanisms of biofilm embedded microorganisms. Microbial biofilms: importance and applications. IntechOpen:189–209. https://doi.org/10.5772/62943
Navidifar T, Amin M, Rashno M (2019) Effects of sub-inhibitory concentrations of meropenem and tigecycline on the expression of genes regulating pili, efflux pumps and virulence factors involved in biofilm formation by Acinetobacter baumannii. Infection and Drug Resistance 12:1099–1111. https://doi.org/10.2147/IDR.S199993
Toska J, Ho BT, Mekalanos JJ (2018) Exopolysaccharide protects Vibriocholerae from exogenous attacks by the type 6 secretion system. Proceedings of the National Academy of Sciences 115(31):7997–8002. https://doi.org/10.1073/pnas.1808469115
Grande R, Puca V, Muraro R (2020) Antibiotic resistance and bacterial biofilm. 30(12):897–900. https://doi.org/10.1080/13543776.2020.1830060
Bowler PG (2018) Antibiotic resistance and biofilm tolerance: a combined threat in the treatment of chronic infections. Journal of Wound Care 27(5):273–277. https://doi.org/10.12968/jowc.2018.27.5.273
Pizzolato-Cezar LR, Okuda-Shinagawa NM, Machini MT (2019) Combinatory therapy antimicrobial peptide-antibiotic to minimize the ongoing rise of resistance. Frontiers in Microbiology 10:1703. https://doi.org/10.3389/fmicb.2019.01703
Wu X, Li Z, Li X, Tian Y, Fan Y, Yu C, Zhou B, Liu Y, Xiang R, Yang L (2017) Synergistic effects of antimicrobial peptide DP7 combined with antibiotics against multidrug-resistant bacteria. Drug Design, Development and Therapy 11:939. https://doi.org/10.2147/DDDT.S107195.
Sengupta D, Datta S, Biswas D (2020) Surfactant exopolysaccharide of Ochrobactrum pseudintermedium C1 has antibacterial potential: Its bio-medical applications in vitro. Microbiological Research 236:126466. https://doi.org/10.1016/j.micres.2020.126466
Spanò A, Laganà P, Visalli G, Maugeri TL, Gugliandolo C (2016) In vitro antibiofilm activity of an exopolysaccharide from the marine thermophilic Bacillus licheniformis T14. Current Microbiology 72(5):518–528. https://doi.org/10.1007/s00284-015-0981-9
Tkhilaishvili T, Lombardi L, Klatt A-B, Trampuz A, Di Luca M (2018) Bacteriophage Sb-1 enhances antibiotic activity against biofilm, degrades exopolysaccharide matrix and targets persisters of Staphylococcus aureus. International journal of antimicrobial agents 52(6):842–853. https://doi.org/10.1016/j.ijantimicag.2018.09.006
El-Wafa A, Mohamed W, Ahmed RH, Ramadan MA-H (2020) Synergistic effects of pomegranate and rosemary extracts in combination with antibiotics against antibiotic resistance and biofilm formation of Pseudomonas aeruginosa. Brazilian Journal of Microbiology 51:1079–1092. https://doi.org/10.1007/s42770-020-00284-3
Singh PK, Parsek MR, Greenberg EP, Welsh MJ (2002) A component of innate immunity prevents bacterial biofilm development. Nature 417(o.6888):552–555. https://doi.org/10.1038/417552a
Kumar A (2016) House of cellulose-a new hideout for drug tolerant Mycobacterium tuberculosis. Microbial Cell 3(7):299–301. https://doi.org/10.15698/mic2016.07.515
