Multimetal resistance and tolerance in microbial biofilms

Nature Reviews Microbiology

Volumn 5, Issue 12, 2007, Pages 928-938

  Harrison, Joe J ^a   Ceri, Howard ^a   Turner, Raymond J ^a  

^a UNIVERSITY OF CALGARY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ARSENIC; CADMIUM; CATALASE; CHELATING AGENT; CHROMIUM; CIPROFLOXACIN; COBALT; COPPER; DIPICOLINIC ACID; GLUTAREDOXIN; GLUTATHIONE OXIDOREDUCTASE; GLUTATHIONE REDUCTASE; GLUTATHIONE SYNTHASE; INORGANIC COMPOUND; LEAD; MERCURY; METAL; NICKEL; PYOVERDINE; PYRIDINE 2,6 DIMONOTHIOCARBOXYLIC ACID; RUTHENIUM; SELENIUM; SIDEROPHORE; SILVER; SUPEROXIDE DISMUTASE; TELLURIUM; THIOREDOXIN; UNCLASSIFIED DRUG; URANIUM; ZINC;

BACTERIAL COLONIZATION; BACTERIOPLANKTON; BIOFILM; BIOSORPTION; DOSE TIME EFFECT RELATION; ELECTRON TRANSPORT; FENTON REACTION; GENE REARRANGEMENT; GEOCHEMISTRY; INDUSTRIALIZATION; LIGAND BINDING; MEMBRANE TRANSPORT; MICROBIAL POPULATION DYNAMICS; MUTATIONAL ANALYSIS; NONHUMAN; OXIDATION REDUCTION REACTION; PHENOTYPIC VARIATION; PHYSICAL CHEMISTRY; PHYSIOLOGY; POLLUTION; POPULATION STRUCTURE; PRIORITY JOURNAL; QUORUM SENSING; REVIEW; SIGNAL TRANSDUCTION;

BACTERIA; BACTERIAL PHYSIOLOGY; BIOFILMS; DRUG RESISTANCE, MULTIPLE, BACTERIAL; METALS, HEAVY; PHENOTYPE; SIGNAL TRANSDUCTION;

EID: 36248981481     PISSN: 17401526     EISSN: None     Source Type: Journal    
DOI: 10.1038/nrmicro1774     Document Type: Review

References (104)

1. Hall-Stoodley, L., Costerton, J. W. & Stoodley, R Bacterial biofilms: from the natural environment to infectious diseases. Nature Rev. Microbiol. 2, 95-108 (2004).
2. Harrison, J. J. Turner, R. J., Marques, L. L. R. & Ceri, H. Biofilms: A new understanding of these microbial communities is driving a revolution that may transform the science of microbiology. Am. Sci. 93, 508-515 (2005).
3. Battin, T. J. et al. Microbial landscapes: New paths to biofilm research. Nature Rev. Microbiol. 5, 76-81 (2007).
4. Costerton, J. W., Stewart, P. S. & Greenberg, E. P. Bacterial biofilms: a common cause of persistent infections. Science 284, 1318-1322 (1999).
5. Purevdorj-Gage, B., Costerton, W. J. & Stoodley, P. Phenotypic differentiation and seeding dispersal in non-mucoid and mucoid Pseudomonas aeruginosa biofilms. Microbiology 151 1569-1576 (2005).
6. Southey-Pillig, C. J., Davies, D. G. & Sauer. K. Characterization of temporal protein production in Pseudomonas aeruginosa biofilms. J. Bacteriol. 187, 8114-8126 (2005).
7. Haagensen, J. A. J. et al. Differentiation and distribution of colistin- and sodium dodecyl sulfate-tolerant cells in Pseudomonas aeruginosa biofilms. J. Bacteriol. 189, 28-37 (2007),
8. Lewis, K. Persister cells, dormancy and infectious disease. Nature Rev. Microbiol. 5, 48-56 (2007).
9. Bjarnsholt, T. et al. Pseudomonas aeruginoso tolerance to tobramycin, hydrogen peroxide and polymorphonuclear leukocytes is quorum-sensing dependent. Microbiology 151, 373-383 (2005).
10. Spoering, A. & Lewis, K. Biofilm and planktonic cells of Pseudomonas aeruginosa have similar resistance to killing by antimicrobials. J. Bacteriol. 183, 6746-6751 (2001).
11. Harrison, J. J., Turner, R. J. & Ceri, H. Persister cells, the biofilm matrix and tolerance to metal cations in biofilm and planktonic Pseudomonas aeruginoso. Environ. Microbiol. 7, 981-994 (2005).
12. Teitzel, G. M. & Parsek, M. R. Heavy metal resistance of biofilm and planktonic Pseudomonas aeruginosa. Appl. Environ. Microbiol. 69 2313-2320 (2003).
13. Harrison. J. J. et al. Metal resistance in Candida biofilms. FEMS Microbiol. Ecol. 55, 479-491 (2006).
14. Stewart, P. S. Mechanisms of antibiotic resistance in bacterial biofilms. Int. J. Med. Microbial. 292, 107-113 (2002).
15. Ramage, G., Saville, S. P, Thomas, P. D. & Lopez-Ribot, J. L. Candida biofilms: An update. Eukaryotic Cell 4, 633-638 (2005).
16. Boles, B. B., Theondel, M. & Singh, P. K. Self-generated diversity produces "insurance effects" in biofilm communities. Proc. Natl Acad. Sci. USA 101, 6630-16635 (2004).
17. Davies, J. A. et al. The GacS sensor kinase controls phenotypic reversion of small colony variants isolated from biofilms of Pseudomonas aeruginosa PA14. FEMS Microbiol. Ecol. 59, 32-46 (2007).
18. Harrison. J. J. et al. Persister cells mediate tolerance to metal oxyanions in Escherichia coli. Microbiology 151, 3181-3195 (2005).
19. Holm, O., Hansen, E., Lassen, C., Stuer-Lauridsen, F. & Kjolholt, J. European Commission DG ENV. E3, Heavy Metals in Waste - Final Report (COM Consulting Engineers, Denmark, 2002).
20. Munoz, R. et al. Sequential removal of heavy metal ions and organic pollutants using an algal-bacterial consortium. Chemosphere 63, 903-911 (2006).
21. Singh, R., Paul, D. & Jain, R. Biofilms: Implications in bioremediation. Trends Microbiol. 14, 389-397 (2006).
22. Diels, L. et al. Heavy metals removal by sand filters inoculated with metal sorbing and precipitating bacteria. Hydrometallurgy 71, 235-241 (2003).
23. Chang, W. C., Hsu, G. S., Chiang, S. M. & Su. M. C. Heavy metal removal from aqueous solution by wasted biomass from a combined AS-biofilm process. Bioresour. Technol. 97, 1503-1508 (2006).
24. Anderson, C., Pederson, K. & Jakobsson, A. M. Autoradiographic comparisons of radionuclide adsorption between subsurface anaerobic biofilms and granitic host rocks. Geomicrobiol. J. 23, 15-29 (2006).
25. Rawlings. D. E. & Johnson, D. B: The microbiology of blomining: development and Optimization of mineral oxidizing microbial consortia. Microbiology 153, 315-324 (2007).
26. Lawrence, J. R. et al. Microscale and molecular assessment of impacts of nickel, nutrients, and oxygen level on structure and function of river biofilm communities. Appl. Environ. Microbiol. 70, 4326-4339 (2004).
27. Vilchez, R. Pozo, C., Gomez, M. A., Rodelas, B. & Gonzalez-Lopez, J. Dominance of spbingomonads in a copper exposed biofilm community for groundwater treatment. Microbiology 153, 325-337 (2007).
28. Nieboer, E. & Fletcher, G. G. in Toxicology of Metals (ed. Chang, L W) 113-132 (CRC, Boca Raton, 1996).
29. Stohs, S. J. & Bagchi, D. Oxidative mechanisms in the toxicity of metal ions. Free Radic. Biol. Med. 18, 321-336 (1995).
30. Zannoni, D., Borsetti, F., Harrison, J. J. & Turner, R. J. The bacterial response to the chalcogen metalloids Se and Te. Adv. Microb. Physiol. 53, 1-71 (2007).
31. Turner. R. J., Aharonowitz, Y, Weiner, J. & Taylor, D.E. Glutathione is a target of tellurite toxicity and is protected by tellurite resistance determinants in Escherichia coli. Can. J. Microbiol. 47, 33-40 (2001).
32. Tremaroli, V., Fedi, S. & Zannoni, D. Evidence for a tellurite-dependent generation of reative oxygen species and absence of a tellurite-mediated adaptive response to oxidative stress in cells of Pseudomonas pseudoalcaligenes KF707. Arch. Microbiol. 187, 127-135 (2007).
33. Kessi. J. & Hanselmann, K. W. Similarities between the abiotic reduction of selenite with glutathione and the dissimilatory reaction mediated by Rhodospirillum rubrum and Escherichia coli. J. Biol. Chem. 279, 50662-50669 (2004).
34. Geslin, C., Lianos, J., Prieur, D. & Jeanthon, C. The manganese and iron superoxide dismutases protect Escherichia coli from heavy metal toxicity. Res. Microbiol. 152, 901-905 (2091).
35. Inoaoka. T, Matsumura. Y. & Tsuchido, T SodA and manganese are essential for resistance to oxidative stress in growing and sporulating cells of Bacillus subtillis. J. Bacteriol. 181, 1939-1943 (1999).
36. Pomposiello, P.J. & Demple, B, Global adjustment of microbial physiology during free radical stress. Adv Microb. Physiol. 46, 319-341 (2002).
37. Foulkes, E. C. Biological membranes in toxicology (Taylor & Francis, Philadelphia. 1998).
38. 2-) on the plasma membrane redox system of the facultative phototroph Rhodobacter capsulatus. J. Bacteriol. 189, 851-859 (2007).
39. 31P nuclear magnetic resonance investigation of tellurite toxicity in Escherichia coli. Appl. Environ. Microbiol. 70, 7342-7347 (2004).
40. Workentine, M. L., Harrison, J. J. Stenroos, P. U., Ceri, H. & Turner, R. J. Peudomonas fluorescens' view of the periodic table. Environ. Microbiol. (in the press).
41. Nies, D. H. Efflux-mediated heavy metal resistance in prokaryotes. FEMS Microbiol. Rev. 27, 313-339 (2003).
42. Xu, K. D. Stewart, P. S., Xia, F., Huang; C. & McFeters, G. A. Spatial physiological heterogeneity in Pseudomonas aeruginosa biofilm is determined by oxygen availability. Appl. Environ. Microbiol. 64 4035-4039 (1998).
43. Werner, E. et al. Stratified growth in Pseudomonas aeruginosa biofilm. Appl. Environ. Microbiol. 70, 6188-6196 (2004).
44. Huang. C. Xu, K. D., McFeters, G. A. & Stewart. P. S. Spatial patterns of alkaline phosphatase expression within bacterial colopies and biofilms in response to phosphate starvation. Appl. Environ. Microbiol. 64, 1526-1531 (1998).
45. Pringaalt O., Epping, L, Guyoneaud, R., Khalili. A. & Kuhl, M. Dynamics of anoxygenic photosynthesis in an experimental green sulphur bacteria biofilm. Environ. Microbiol. 1, 295-305 (1999).
46. Hunter, R. C. & Beveridge. T. J. Application of a pH-sensitive fluoroprobe (C-SNARF-4) for pH microenvironment analysis in Pseudomonas aeruginosa biofilms. Appl. Environ, Microbiol. 71, 2501-2510 (2005).
47. Rani, S. A. et al. Spatial patterns of DNA replication, protein synthesis and oxygen concentration within bacterial biofilms reveal diverse physiological states. J Bacteriol. 189, 4223-4233 (2007).
48. Xu, K. D., McFeters, G. A. & Stewart, P. S. Biofilm resistance to antimicrobial agents. Microbiology 146, 547-549 (2000).
49. Bordello, G. et al. Oxygen limitation contributes to antibiotic tolerance of Pseudomonas aeruginosa in biofilms. Antimicrob. Agents Chemother. 48, 2659-2664 (2004).
50. Walters III, M. C., Roe, F., Bugnicourt, A., Franklin, M. J. & Stewart, P. S. Contributions of antibiotic penetration, oxygen limitation, and low metabolic activity to tolerance of Pseudomonas aeruginosa biofilms to ciproffoxacin and tobramycin. Antimicrob. Agents Chemorther. 47, 317-323 (2003).
51. Lafleur, M. D., Kumamoto, C. A. & Lewis, K. Candida albicans biofilms produce antifungal tolerant persister cells. Antimicrob. Agents Chemother. 50, 3839-3846 (2006).
52. Harrison. J. J. et al. Metal ions may supress or enhance cellular differentiation in Candida albicans and Candida tropicalis biofilms. Appl. Environ. Microbiol. 73, 4940-4949 (2007).
53. Harrison, J. J., Turner, R. J. & Ceri, H. A subpopulation of Candida albicans and Candida tropicalis biofilm cells are highly tolerant to chelating agents. FEMS Microbiol. Lett. 272, 172-181 (2007).
54. Harrison, J. J. et al. Effects of the twin-arginine translocase on the structure and antimicrobial susceptibility of Eschenchia coli biofilms. Can. J. Microbiol. 51, 671-683 (2005).
55. Harrison, J. J. et al. The use of microscopy and three-dimensional visualization to evaluate the structure of microbial biofilms cultivated in the Calgary Biofilm Device. Biol. Proced. Online 8, 194-215 (2006).
56. Shrout, J. D. et al. The impact of quorum-sensing and swarming motility on Pseudomonas aeruginoso biofilm formation is nutritionally conditional. Mol. Microbiol. 62, 1264-1277 (2006).
57. Kirisits, M.J. & Parsek, M. R. Does Pseudomonas aeruginosa use intercellular signalling to build biofilm communities? Cell. Microbiol. 8, 1841-1849 (2006).
58. Hassett, D. J. et al. Quorum sensing in Pseudomonas aeruginoso controls expression of catalase and superoxide dismutase genes and mediates biofilm susceptibility to hydrogen peroxide. Mol. Microbiol. 34, 1082-1093 (1999).
59. Teitzel, G. M. et al. Survival and growth in the presence of elevated copper: Transcriptional profiling of copper-stressed Pseudomonas aeruginosa. J. Bactenol. 188, 7242-7256 (2006).
60. Parvatiyar, K. et al. Global analysis of cellular factors and responses involved in Pseudomonas aeruginosa resistance to arsenite. J. Bacteriol. 187, 4853-4864 (2005).
61. Harrison, J. J., Ceri, H., Stremick, C. & Turner, R. J. Differences in biofilm and planktonic cell mediated reduction of metalloid oxyanions. FEMS Microbiol. Lett. 235, 357-362 (2004).
62. van Hullebusch, E. D., Zandvoort, M. H. & Lens, P. N. L. Metal immobilization by biofilms: Mechanisms and analytical tools. Rev. Environ. Sci. Biotechnol. 2, 9-33 (2003).
63. Tabak, H. H., Lens, P., van Hullebusch. E. D. & Dejonghe, W. Developments in bioremediation of soils and sediments polluted with metals and radionuclides - 1. Microbial processes and mechanisms affecting bioremediation of metal contamination and influencing metal toxicity and transport. Rev. Environ. Sci. Biotechnol. 4, 115-156 (2005).
64. Mages, M., Ovari, M., Tumpling, W. & Kropfi, K. Biofilms as bio-indicator for polluted waters? Total reflection X-ray fluorescence analysis of biofilms of the Tisza river (Hungary). Anal. Bioanal. Chem. 378, 1095-1101 (2004).
65. Dupraz, C. & Visscher, P. T. Microbial lithification in marine stromatolites and hypersaline mats. Trends Microbiol. 13, 429-438 (2005).
66. Whitchurch, C. B., Tolker-Neilsen, T., Ragas, R C. & Mattick, J. S. Extracellular DNA required for bacterial biofilm formation. Science 295, 1487 (2002).
67. Branda, S. S., Chu, F., Kearns, D. B., Losick. R. & Kolter, R. A major protein component of the Bacillus subtilis biofilm matrix. Mol. Microbiol. 59, 1229-1238 (2006).
68. Branda, S. S., Vik, S., Friedman, L. & Kolter, R. Biofilms: The matrix revisited. Trends Microbiol. 13, 20-26 (2005).
69. Sutherland, I. W. Biofilm exopolysaccharides: A strong and sticky framework. Microbiology 147. 3-9 (2001).
70. Liu. H. & Fang, H. P. Characterization of electrostatic binding sites of extracellular polymers by linear programming analysis of titration data. Biotechnol. Bioeng. 80, 806-811 (2002).
71. Stewart, P. S. Diffusion in biofilms. J. Bacteriol. 185, 1485-1491 (2003).
72. Römling, U., Gomelsky, M. & Galperin, M. Y. C-di-GMP: The dawning of a novel bacterial signaling system. Mol. Microbiol. 57, 629-639 (2005).
73. Drenkard, E. & Ausubel, F. M. Pseudomonas biofilm formation and antibiotic resistance are linked to pheaotypic variation. Nature 416, 740-743 (2002).
74. Hu, Z. et al. Determination of spatial distributions of zinc and active biomass in microbial biofilms by two-photon laser scanning microscopy. Appl. Environ. Microbiol. 71, 4014-4021 (2005).
75. Hu. Z. et al. Spatial distributions of copper in microbial biofilms by scanning electrochemical microscopy. Environ. Sci. Technol. 41, 936-941 (2007).
76. Langley, S. & Beveridge, T. J. Metal binding by Pseudomonas aeruginosa PAO1 is influenced by growth ofthe cells as a biofilm. Can. J. Microbiol. 45, 616-622 (1999).
77. Schooling, S. R. & Beveridge, T. J. Membrane vesicles: An-overlooked component of the matrices of biofilms. J. Bacteriol. 188, 5945-5957 (2006).
78. Kirisitis, M. J., Prost, L., Starkey, M. & Parsek, M. Characterization of colony morphology variants isolated from Pseudomonas aeruginosa biofilms. Appl. Environ. Microbiol. 71, 4809-4821 (2005).
79. Haussler, S. Biofilm formation by the small colony variant phenotype or Pseudomonas aeruginosa. Environ. Microbiol. 6, 546-551 (2004).
80. Beyenal. H. et al. Uranium immobilization by sulfate reducing biofilms. Environ. Sci. Technol. 38, 2067-2074 (2004).
81. Beyenal, H. & Lewandowski, Z. Dynamics of lead immobilization in sulfate reducing biofilms. Water Res. 38, 2726-2736 (2004).
82. Toner, B., Fakra, S., Villalobos, M., Warwick, T. & Sposito. G. Spatially resolved characterization of biogenic manganese oxide production within a bacterial biofilm. Appl. Environ. Microbiol. 71, 1300-1310 (2005).
83. Stintzi, A., Evans, K., Meyer, J. M. & Poole. K. Quorum-sensing and siderophore biosynthesis in Pseudomonas aeruginosa: LasR/lasl mutants exhibit reduced pyoverdine synthesis. FEMS Microbiol. Lett. 166 341-345 (1998).
84. Cortese, M. S. et al. Metal chelating properties of pyridine-2,6-bis(thiocarboxylic acid) produced by Pseudomonas spp. and the biological activities or the formed complexes. Biometals 15, 103-120 (2002).
85. Zawadzka, K M., Crawford, R. L. & Paszczynski, A. J. Pyridine-2,6-bis(thiorarboxylic acid) produced by Pseudomonas stutzeri KC reduces and precipitates selenium and tellurium oxyanions. Appl. Environ. Microbiol. 72, 3119-3129 (2006).
86. Brown, S. D. et al. Molecular dynamics of the Shewanella oneidensis response to chromate stress. Mol. Cell. Proteomics 5, 1054-1071 (2006).
87. Hu, P., Brodie, E. L., Suzuki, Y., McAdams, H. H. & Andersen, G. L. Whole-genorne transcriptional analysis of heavy metal stresses in Caulobacter crescentus. J. Bacteriol. 187, 8437-8449 (2005).
88. Szomolay, B., Klapper, I., Dockery, J. & Stewart, R S. Adaptive responses to antimicrobial agents in biofilms. Environ. Microbiol. 7, 1186-1191 (2005).
89. Lewis, K. Riddle of biofilm resistance. Antimicrob. Agents Chemother. 45, 999-1007 (2001),
90. Kaneko, Y., Theondel, M., Olakanmi, O., Britigan. B. E. & Singh, P. K. The transition metal gallium disrupts Pseudomonas aeruginosa iron metabolism and has antimicrobial and antibiofilm activity. J. Clin. Invest. 117, 877-888 (2007).
91. Keren, I., Shah, D., Spoering,A., Kaldalu, N. & Lewis. K. Specialized persister cells and the mechanism of multidrug tolerance in Escherichia coli. J. Bacteriol. 186, 8172-8180 (2004).
92. Shah, D. et al. Persisters: A distinct physiological state of E. coli. BMC Microbiol. 6, 53 (2006).
93. Korch., S. B., Henderson, T. A. & Hill, T. M. Characterization of the hipA7 allele of Eschenchia coli and evidence that high persistence is governed by (p)ppGpp synthesis. Mol. Microbiol. 50, 1199-1213 (2003).
94. van den Broek, D., Bloemberg, G. V. & Lugtenberg, B. J. The role of phenotypic variation in rhizosphere Pseudomonas bacteria. Environ. Microbiol. 7, 1686-1697 (2005).
95. Venturi, V. Regulation of quorum sensing in Pseudomonas. FEMS Microbiol. Rev. 30, 274-291 (2006).
96. Duffy, B. K. & Defago, G. Controlling instability in gocS-gocA regulatory genes during inoculant production of Pseudomonas fluorescens biocontrol strains. Appl. Environ. Microbiol. 66 3142-3150 (2000).
97. Sánchez-Contreras, M. et al. Phenotypic selection and phase variation occur during alfalfa root colonization by Pseudomonas fluorescens F113. J. Bacterial. 184, 1587-1596 (2002).
98. Martinez-Granero, F., Capdevila, S., Sánchez-Contreras, M., Martin, M. & Rivilla, R. Two site-specific recombinases are implicated in phenotypic variation and competitive rhizosphere colonization in Pseudomonas fluorescens. Microbiology 151, 975-983 (2005).
99. Gorby, Y. A. et al. Electrically conductive bacterial nanowires produced by Shewanella oneidensis strain MR-1 and other microorganisms. Proc. Natl Acad. Sci. USA 103. 11358-11363 (2006).
100. Coby, A. J. & Picardal, F. W. Influence of sediment components on the immobilization of Zn during microbial Fe-(hydr)oxide reduction. Environ. Sci. Technol. 40, 3813-3818 (2006).
101. Wright, M. S., Peltier, G. L., Stapanauskas, R. & McArthur, J. V. Bacterial tolerances to metals and antibiotics in metal contaminated and reference streams. FEMS Micrubiol. Ecol. 58, 293-302 (2006).
102. Baker-Austin, C., Wright, M. S., Stepanauskas, R. & McArthur, J. V. Co-selection of antibiotic and metal resistance. Trends Microbiol. 14, 176-182 (2006).
103. Harrison, J. J., Ceri, H., Stremick, C. & Turner, R. J. Biofilm susceptibility to metal toxicity. Environ. Microbiol. 6, 1220-1227 (2004).
104. Harrison, J. J., Turner, R. J. & Ceri. H. High-throughput metal susceptibility testing of microbial biofilms. BMC Microbiol. 5 53 (2005).