Dual roles of capsular extracellular polymeric substances in photocatalytic inactivation of Escherichia coli: Comparison of E. coli BW25113 and isogenic mutants

Applied and Environmental Microbiology

Volumn 81, Issue 15, 2015, Pages 5174-5183

  Huang, Guocheng ^a   Xia, Dehua ^a   An, Taicheng ^b   Ng, Tsz Wai ^a   Yip, Ho Yin ^a   Li, Guiying ^b   Zhao, Huijun ^c   Wong, Po Keung ^a  

^a CHINESE UNIVERSITY OF HONG KONG   (Hong Kong)

^b GUANGZHOU INSTITUTE OF GEOCHEMISTRY   (China)

^c GRIFFITH UNIVERSITY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIA; CELL MEMBRANES; CYTOLOGY; ESCHERICHIA COLI; FLUORESCENCE MICROSCOPY; POLYMERS; SCANNING ELECTRON MICROSCOPY;

ACID BASE INTERACTION; BACTERIAL RESISTANCE; EXTRACELLULAR POLYMERIC SUBSTANCES; INTERACTION ENERGIES; NANOPARTICLE INTERACTION; PHOTOCATALYTIC INACTIVATIONS; PHOTOCATALYTIC TREATMENT; SCANNING ELECTRONS;

CELLS;

ADHESION; BACTERIUM; CATALYSIS; CELL ORGANELLE; COLIFORM BACTERIUM; MATHEMATICAL ANALYSIS; MUTATION; OXIDE; PARTICULATE MATTER; POLYMER;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI;

PHOTOCHEMICAL SMOG; TITANIUM; TITANIUM DIOXIDE;

BACTERIAL CAPSULE; BACTERIAL LOAD; CYTOLOGY; DRUG EFFECTS; ESCHERICHIA COLI; MICROBIAL VIABILITY; MICROSCOPY; PHOTOCHEMICAL SMOG; PHYSIOLOGY; RADIATION RESPONSE; TOXICITY; ULTRAVIOLET RADIATION;

BACTERIAL CAPSULES; BACTERIAL LOAD; ESCHERICHIA COLI; MICROBIAL VIABILITY; MICROSCOPY; OXIDANTS, PHOTOCHEMICAL; TITANIUM; ULTRAVIOLET RAYS;

EID: 84936973024     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.00775-15     Document Type: Article

References (55)

1. Shannon MA, Bohn PW, Elimelech M, Georgiadis JG, Marinas BJ, Mayes AM. 2008. Science and technology for water purification in the coming decades. Nature 452:301-310. http://dx.doi.org/10.1038/nature06599.
2. 6 nanojunction system: a novel and efficient photocatalyst with double visible-light active components. Appl Catal A Gen 363:221-229. http://dx.doi.org/10.1016/j.apcata.2009.05.028.
3. Chong MN, Jin B, Chow CWK, Saint C. 2010. Recent developments in photocatalytic water treatment technology: a review. Water Res 44:2997-3027. http://dx.doi.org/10.1016/j.watres.2010.02.039.
4. 6 nanojunction system irradiated by visible light: the role of diffusing hydroxyl radicals. Environ Sci Technol 44:1392-1398. http://dx.doi.org/10.1021/es903087w.
5. Chen YM, Lu AH, Li Y, Zhang LS, Yip HY, Zhao HJ, An TC, Wong PK. 2011. Naturally occurring sphalerite as a novel cost-effective photocatalyst for bacterial disinfection under visible light. Environ Sci Technol 45:5689-5695. http://dx.doi.org/10.1021/es200778p.
6. 6 micro/nano-structures: synthesis, modifications and visible-light-driven photocatalytic applications. Appl Catal B Environ 106:1-13. http://dx.doi.org/10.1016/j.apcatb.2011.05.008.
7. Wong MS, Chu WC, Sun DS, Huang HS, Chen JH, Tsai PJ, Lin NT, Yu MS, Hsu SF, Wang SL, Chang HH. 2006. Visible-light-induced bactericidal activity of a nitrogen-doped titanium photocatalyst against human pathogens. Appl Environ Microbiol 72:6111-6116. http://dx.doi.org/10.1128/AEM.02580-05.
8. Dalrymple OK, Stefanakos E, Trotz MA, Goswami DY. 2010. A review of the mechanisms and modeling of photocatalytic disinfection. Appl Catal B Environ 98:27-38. http://dx.doi.org/10.1016/j.apcatb.2010.05.001.
9. 2 photocatalysis and UVA photolysis for the destruction of three pathogenic micro-organisms. J Photochem Photobiol A Chem 175:51-56. http://dx.doi.org/10.1016/j.jphotochem.2005.04.033.
10. 2 crystals. Russ J Phys Chem B 2:105-114. http://dx.doi.org/10.1134/S1990793108010168.
11. 2 photocatalyst. J Nanosci Nanotechnol 11:1551-1554. http://dx.doi.org/10.1166/jnn.2011.3339.
12. Pigeot-Remy S, Simonet F, Errazuriz-Cerda E, Lazzaroni JC, Atlan D, Guillard C. 2011. Photocatalysis and disinfection of water: identification of potential bacterial targets. Appl Catal B Environ 104:390-398. http://dx.doi.org/10.1016/j.apcatb.2011.03.001.
13. Eboigbodin KE, Biggs CA. 2008. Characterization of the extracellular polymeric substances produced by Escherichia coli using infrared spectroscopic, proteomic, and aggregation studies. Biomacromolecules 9:686-695. http://dx.doi.org/10.1021/bm701043c.
14. Gilbert P, Das J, Foley I. 1997. Biofilm susceptibility to antimicrobials. Adv Dent Res 11:160-167.
15. Xue Z, Sendamangalam VR, Gruden CL, Seo Y. 2012. Multiple roles of extracellular polymeric substances on resistance of biofilm and detached clusters. Environ Sci Technol 46:13212-13219. http://dx.doi.org/10.1021/es3031165.
16. Liu Y, Li J, Qiu XF, Burda C. 2007. Bactericidal activity of nitrogendoped metal oxide nanocatalysts and the influence of bacterial extracellular polymeric substances (EPS). J Photochem Photobiol A Chem 190:94-100. http://dx.doi.org/10.1016/j.jphotochem.2007.03.017.
17. Gong AS, Lanzl CA, Cwiertny DM, Walker SL. 2012. Lack of influence of extracellular polymeric substances (EPS) level on hydroxyl radical mediated disinfection of Escherichia coli. Environ Sci Technol 46:241-249. http://dx.doi.org/10.1021/es202541r.
18. Nielsen PH, Jahn A, Palmgren R. 1997. Conceptual model for production and composition of exopolymers in biofilms. Water Sci Technol 36(1):11-19. http://dx.doi.org/10.1016/S0273-1223(97)00318-1.
19. 2 thin films: dynamic view of the active oxygen species responsible for the effect. J Photochem Photobiol A Chem 106:51-56.
20. Mills A, LeHunte S. 1997. An overview of semiconductor photocatalysis. J Photochem Photobiol A Chem 108:1-35. http://dx.doi.org/10.1016/S1010-6030(97)00118-4.
21. 2 photocatalysis involves adsorption onto catalyst and the loss of membrane integrity. FEMS Microbiol Lett 258:18-24. http://dx.doi.org/10.1111/j.1574-6968.2006.00190.x.
22. Cheng CL, Sun DS, Chu WC, Tseng YH, Ho HC, Wang JB, Chung PH, Chen JH, Tsai PJ, Lin NT, Yu MS, Chang HH. 2009. The effects of the bacterial interaction with visible-light responsive Titania photocatalyst on the bactericidal performance. J Biomed Sci 16:7. http://dx.doi.org/10.1186/1423-0127-16-7.
23. 2: effect on the photocatalytic activity for disinfection applications. Catal Today 209:140-146. http://dx.doi.org/10.1016/j.cattod.2012.12.010.
24. Chia TWR, Nguyen VT, McMeekin T, Fegan N, Dykes GA. 2011. Stochasticity of bacterial attachment and its predictability by the extended Derjaguin-Landau-Verwey-Overbeek theory. Appl Environ Microbiol 77:3757-3764. http://dx.doi.org/10.1128/AEM.01415-10.
25. Thabet S, Simonet F, Lemaire M, Guillard C, Cotton P. 2014. Impact of photocatalysis on fungal cells: depiction of cellular and molecular effects on Saccharomyces cerevisiae. Appl Environ Microbiol 80:7527-7535. http://dx.doi.org/10.1128/AEM.02416-14.
26. Baba T, Ara T, Hasegawa M, Takai Y, Okumura Y, Baba M, Datsenko KA, Tomita M, Wanner BL, Mori H. 2006. Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection. Mol Syst Biol 2:2006.0008. http://dx.doi.org/10.1038/msb4100050.
27. Gao MH, An TC, Li GY, Nie X, Yip HY, Zhao H, Wong PK. 2012. Genetic studies of the role of fatty acid and coenzyme A in photocatalytic inactivation of Escherichia coli. Water Res 46:3951-3957. http://dx.doi.org/10.1016/j.watres.2012.05.033.
28. 2 nanotubes as a photoanode. Appl Catal B Environ 147:562-570. http://dx.doi.org/10.1016/j.apcatb.2013.09.037.
29. 2 in the visible-light-driven photocatalytic inactivation of E. coli using natural sphalerite: a genetic study. J Phys Chem B 119:3104-3111. http://dx.doi.org/10.1021/jp511201w.
30. Ratto M, Verhoef R, Suihko ML, Blanco A, Schols HA, Voragen AGJ, Wilting R, Siika-Aho M, Buchert J. 2006. Colanic acid is an exopolysaccharide common to many enterobacteria isolated from paper-machine slimes. J Ind Microbiol Biotechnol 33:359-367. http://dx.doi.org/10.1007/s10295-005-0064-1.
31. Hanna A, Berg M, Stout V, Razatos A. 2003. Role of capsular colanic acid in adhesion of uropathogenic Escherichia coli. Appl Environ Microbiol 69:4474-4481. http://dx.doi.org/10.1128/AEM.69.8.4474-4481.2003.
32. Xia DH, Ng TW, An TC, Li GY, Li Y, Yip HY, Zhao HJ, Lu AH, Wong PK. 2013. A recyclable mineral catalyst for visible-light-driven photocatalytic inactivation of bacteria: natural magnetic sphalerite. Environ Sci Technol 47:11166-11173. http://dx.doi.org/10.1021/es402170b.
33. 2 hollow nanospheres: transformative self-assembly and photocatalytic inactivation of bacteria. ACS Appl Mater Interfaces 6:2405-2412. http://dx.doi.org/10.1021/am4047975.
34. Bergmaier D, Lacroix C, Macedo MG, Champagne CP. 2001. New method for exopolysaccharide determination in culture broth using stirred ultrafiltration cells. Appl Microbiol Biotechnol 57:401-406. http://dx.doi.org/10.1007/s002530100764.
35. Wang WJ, Yu Y, An TC, Li GY, Yip HY, Yu JC, Wong PK. 2012. Visible-light-driven photocatalytic inactivation of E. coli K-12 by bismuth vanadate nanotubes: bactericidal performance and mechanism. Environ Sci Technol 46:4599-4606. http://dx.doi.org/10.1021/es2042977.
36. Chen G, Strevett KA. 2003. Microbial surface thermodynamics and interactions in aqueous media. J Colloid Interface Sci 261:283-290. http://dx.doi.org/10.1016/S0021-9797(02)00242-4.
37. 2-explanation by DLVO and XDLVO theory. Water Res 47:1503-1511. http://dx.doi.org/10.1016/j.watres.2012.11.030.
38. Wang LX, Xu SP, Li J. 2011. Effects of phosphate on the transport of Escherichia coli O157:H7 in saturated quartz sand. Environ Sci Technol 45:9566-9573. http://dx.doi.org/10.1021/es201132s.
39. Bayoudh S, Othmane A, Mora L, Ben Ouada H. 2009. Assessing bacterial adhesion using DLVO and XDLVO theories and the jet impingement technique. Colloid Surf B Biointerfaces 73:1-9. http://dx.doi.org/10.1016/j.colsurfb.2009.04.030.
40. Gottesman S, Stout V. 1991. Regulation of capsular polysaccharide synthesis in Escherichia coli K12. Mol Microbiol 5:1599-1606. http://dx.doi.org/10.1111/j.1365-2958.1991.tb01906.x.
41. Schmitt J, Flemming HC. 1998. FTIR-spectroscopy in microbial and material analysis. Int Biodeterior Biodegradation 41:1-11.
42. 2 interface by ATR-FTIR and laser kinetic spectroscopy. Langmuir 21:4631-4641. http://dx.doi.org/10.1021/la046983l.
43. Badireddy AR, Korpol BR, Chellam S, Gassman PL, Engelhard MH, Lea AS, Rosso KM. 2008. Spectroscopic characterization of extracellular polymeric substances from Escherichia coli and Serratia marcescens: suppression using sub-inhibitory concentrations of bismuth thiols. Biomacromolecules 9:3079-3089. http://dx.doi.org/10.1021/bm800600p.
44. Nelson DL, Cox MM. 2004. Lehninger principles of biochemistry, 4th ed. WH Freeman, New York, NY.
45. Pigeot-Remy S, Simonet F, Atlan D, Lazzaroni JC, Guillard C. 2012. Bactericidal efficiency and mode of action: a comparative study of photochemistry and photocatalysis. Water Res 46:3208-3218. http://dx.doi.org/10.1016/j.watres.2012.03.019.
46. Alakomi HL, Matto J, Virkajarvi I, Saarela M. 2005. Application of a microplate scale fluorochrome staining assay for the assessment of viability of probiotic preparations. J Microbiol Methods 62:25-35. http://dx.doi.org/10.1016/j.mimet.2005.01.005.
47. Liou JW, Gu MH, Chen YK, Chen WY, Chen YC, Tseng YH, Hung YJ, Chang HH. 2011. Visible light responsive photocatalyst induces progressive and apical-terminus preferential damages on Escherichia coli surfaces. PLoS One 6:e19982. http://dx.doi.org/10.1371/journal.pone.0019982.
48. 2 photocatalysis damages lipids and proteins in Escherichia coli. Appl Environ Microbiol 80:2573-2581. http://dx.doi.org/10.1128/AEM.03995-13.
49. Imlay JA. 2003. Pathways of oxidative damage. Annu Rev Microbiol 57:395-418. http://dx.doi.org/10.1146/annurev.micro.57.030502.090938.
50. Tong MP, Ding JL, Shen Y, Zhu PT. 2010. Influence of biofilm on the transport of fullerene (C-60) nanoparticles in porous media. Water Res 44:1094-1103. http://dx.doi.org/10.1016/j.watres.2009.09.040.
51. Lerner RN, Lu QY, Zeng HB, Liu Y. 2012. The effects of biofilm on the transport of stabilized zerovalent iron nanoparticles in saturated porous media. Water Res 46:975-985. http://dx.doi.org/10.1016/j.watres.2011.11.070.
52. Jiang XJ, Wang XT, Tong MP, Kim H. 2013. Initial transport and retention behaviors of ZnO nanoparticles in quartz sand porous media coated with Escherichia coli biofilm. Environ Pollut 174:38-49. http://dx.doi.org/10.1016/j.envpol.2012.11.016.
53. Luef B, Fakra SC, Csencsits R, Wrighton KC, Williams KH, Wilkins MJ, Downing KH, Long PE, Comolli LR, Banfield JF. 2013. Iron-reducing bacteria accumulate ferric oxyhydroxide nanoparticle aggregates that may support planktonic growth. ISME J 7:338-350. http://dx.doi.org/10.1038/ismej.2012.103.
54. Sakimoto KK, Liu C, Lim J, Yang P. 2014. Salt-induced self-assembly of bacteria on nanowire arrays. Nano Lett 14:5471-5476. http://dx.doi.org/10.1021/nl502946j.
55. Chen KL, Bothun GD. 2014. Nanoparticles meet cell membranes: probing nonspecific interactions using model membranes. Environ Sci Technol 48:873-880. http://dx.doi.org/10.1021/es403864v.