Mineralogical variables that control the antibacterial effectiveness of a natural clay deposit

Environmental Geochemistry and Health

Volumn 36, Issue 4, 2014, Pages 613-631

  Morrison, Keith D ^a   Underwood, Jennifer C ^b   Metge, David W ^b   Eberl, Dennis D ^b   Williams, Lynda B ^a  

^a ARIZONA STATE UNIVERSITY   (United States)

^b U S GEOLOGICAL SURVEY   (United States)

Author keywords

Antibacterial; Bacteria; Clays; Iron redox; Pathogens; Pyrite

Indexed keywords

ANTIBIOTIC RESISTANCE; ANTIMICROBIAL ACTIVITY; BACTERIUM; CLAY; CLAY MINERAL; IRON; MINERALOGY; PATHOGEN; PYRITE; REDOX POTENTIAL;

CRATER LAKE; OREGON; UNITED STATES;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; STAPHYLOCOCCUS EPIDERMIDIS;

ALUMINUM; ALUMINUM SILICATE; ANTIINFECTIVE AGENT; CATION; CLAY; IRON; MINERAL; PYRITE; SULFIDE;

CHEMISTRY; DRUG EFFECTS; ESCHERICHIA COLI; MICROBIAL SENSITIVITY TEST; OXIDATION REDUCTION REACTION; PH; SCANNING TRANSMISSION ELECTRON MICROSCOPY; STAPHYLOCOCCUS EPIDERMIDIS; UNITED STATES; X RAY DIFFRACTION;

ALUMINUM; ALUMINUM SILICATES; ANTI-BACTERIAL AGENTS; CATIONS; ESCHERICHIA COLI; HYDROGEN-ION CONCENTRATION; IRON; MICROBIAL SENSITIVITY TESTS; MICROSCOPY, ELECTRON, SCANNING TRANSMISSION; MINERALS; OREGON; OXIDATION-REDUCTION; STAPHYLOCOCCUS EPIDERMIDIS; SULFIDES; X-RAY DIFFRACTION;

EID: 84903152629     PISSN: 02694042     EISSN: None     Source Type: Journal    
DOI: 10.1007/s10653-013-9585-0     Document Type: Article

References (82)

1. Alleva, R., Nasole, E., Di Donato, F., Borghi, B., Neuzil, J., & Tomasetti, M. (2005). α-Lipoic acid supplementation inhibits oxidative damage accelerating chronic wound healing in patients undergoing hyperbaric oxygen therapy. Biochemical and Biophysical Research Communications, 300, 404-410.
2. Anastácio, A. S., Harris, B., Yoo, H., Fabris, J. D., & Stucki, J. W. (2008). Limitations of the ferrozine method for quantitative assay of mineral systems for ferrous and total iron. Geochimica et Cosmochimica Acta, 72, 5001-5008.
3. Aran, D., Maul, A., & Masfaraud, J. (2008). A spectrophotometric measurement of soil cation exchange capacity based on cobaltihexamine chloride absorbance. C. R. Geoscience, 340, 865-871.
4. Aruoma, O. I., Halliwell, B., Laughton, M. J., Quinlan, G. J., & Gutteridge, J. M. C. (1989). The mechanism of interaction of lipid peroxidation. Evidence against a requirement for an iron(II)-iron(III) complex. Biochemisrty Journal, 258, 617-620.
5. Bacon, C. R. (2008). Geologic map of Mount Mazama and Crater Lake caldera, Oregon. U. S Geological Survey Scientific Investigations Map, 2832, 1-47.
6. Bhowal, S., & Chakraborty, R. (2011). Five novel acid-tolerant oligotrophic thiosulfate-metabolizing chemolithotrophic acid mine drainage strains affiliated with the genus Burkholderia of Betaproteobacteria and identification of two novel soxB gene homologues. Research in Microbiology, 162, 436-445.
7. Borrok, D., Fein, J. B., Tischler, M., O'Loughlin, E., Meyer, H., Liss, M., et al. (2004). The effect of acidic solutions and growth conditions on the adsorptive properties of bacterial surfaces. Chemical Geology, 209, 107-119.
8. Brunet de Courrsou L. (2002). Study Group Report on Buruli ulcer treatment with clay, 5th WHO Advisory Group Meeting on Buruli Ulcer, Geneva, Switzerland.
9. Bullen, J. J., Rogers, H. J., Spalding, P. B., & Ward, C. G. (2006). Natural resistance, iron and infection: A challenge for clinical medicine. Journal of Medical Microbiology, 55, 251-258.
10. Cabiscol, E., Tamarit, J., & Ros, J. (2000). Oxidative stress in bacteria and protein damage by reactive oxygen species. International Microbiology, 3, 3-8.
11. Cadet, J., Delatour, T., Douki, T., Gasparutto, D., Pouget, J. P., Ravanat, J. L., et al. (1999). Hydroxyl radicals and DNA base damage. Mutation Research, 424, 9-21.
12. Carretaro, M. I. (2002). Clay minerals and their beneficial effects upon human health. A review. Applied Clay Science, 21, 155-163.
13. Church, C. D., Wilkin, R. T., Alpers, C. N., Rye, R. O., & McCleskey, R. B. (2007). Microbial sulfate reduction and metal attenuation in pH 4 acidic mine water. Geochemical Transictions, 8, 1-14.
14. Cohn, C. A., Laffers, R., Simon, S. R., O'Riordan, T., Schoonen, & M. A. A. (2006). Role of pyrite in formation of hydroxyl radicals in coal: Possible implications for human health. Particle and Fibre Toxic, 3(article 16), 1-10.
15. Cunningham, T. B., Koehl, J. L., Summers, J. S., & Haydel, S. E. (2010). pH-dependent metal ion toxicity influences of the antibacterial activity of two natural mineral mixtures. PLoS-ONE, 5, e9456.
16. Derkowski, A., & Bristow, T. F. (2012). On the problems of total specific surface area and cation exchange capacity measurements in organic-rich sedimentary rocks. Clays and Clay Minerals, 60, 348-362.
17. Dick, J. M. (2008). Calculation of the relative metastabilities of proteins using the CHNOSZ software package. Geochemical Transactions, 9(10), 1-17.
18. Dold, B. (2005). Basic concepts in environmental geochemistry of sulfide mine-waste, Del 22 de Agosto al 2 de Sept. XXIV Curso Latinoamericano de Metalogenia UNESCO-SEG.
19. Eberl, D. D. (2007). User's guide to rockjock: A program for determining quantitative mineralogy from powder X-ray diffraction data. U. S. Geological Survey, Open-file report 03-78.
20. Evangelou, V. P. (1995). Pyrite oxidation and its control. New York: CRC Press.
21. Fang, F. C. (2004). Antimicrobial reactive oxygen and nitrogen species: Concepts and controversies. Nature Reviews Microbiology, 2, 820-832.
22. Ferrell, R. E. (2008). Medicinal clay and spiritual healing. Clays and Clay Minerals, 56, 751-760.
23. Ferrero, T. (1992). Geologic mapping and sampling project, Foster Creek sulfur deposit. Company Report, Ferrero Geologic, 340 Avery St. Ashland Oregon, 97520.
24. Galan, E., Carretero, M. I., & Fernandez-Caliani, J. C. (1999). Effects of acid mine drainage on clay minerals suspended in the Tinto River (Río Tinto, Spain). An experimental approach. Clay Minerals, 34, 99-108.
25. Garrels, R. M., & Thompson, M. E. (1960). Oxidation of pyrite by iron sulfate solutions. American Journal of Science, 258-A, 57-67.
26. Gethin, G. T. (2007). The significance of surface pH in chronic wounds. Wounds UK, 3, 52-56.
27. Gethin, G. T., Cowman, S., & Conroy, R. M. (2008). The impact of Manuka honey dressings on the surface pH of chronic wounds. International Wound Journal, 5, 185-194.
28. Götz, F. (2002). Staphylococcus and biofilms. Molecular Microbiology, 43, 1367-1378.
29. Gutteridge, J. M. C. (1995). Lipid peroxidation and antioxidants as biomarkers of tissue damage. Clinical Chemistry, 41, 1819-1828.
30. Halliwell, B., & Chirico, S. (1993). Lipid peroxidation: Its mechanism, measurement, and significance. American Journal of Clinical Nutrition, 57, 715s-725s.
31. Hanaichi, T., Sato, T., Iwamoto, T., Malavasi-Yamashiro, J., Hoshing, M., & Mizuno, N. (1986). A stable lead by modification of Sato's method. Journal of Electron Microscopy, 35, 304-306.
32. Harrison, J. J., Turner, R. J., & Ceri, H. (2005). High-throughput metal susceptibility testing of microbial biofilms. BMC Microbiology, 5, 1-11.
33. Hutchinson, I. P. G., & Ellison, R. D. (1992). Mine waste management. Lewis publishers, INC. 121 S. Main St. Chelsea, Michigan.
34. Isakow, W., & Micek, S. T. (2006). Methicillin-resistant staphylococcus aureus pneumonia-current and furute therapeutic options. US Respiratory Disease 62-64.
35. Kaufman, T., Eichenlaub, E. H., Angel, M. F., Levin, M., & Futrell, J. W. (1985). Topical acidification promotes healing of experimental deep partial thickness skin burns: A randomized double-blind preliminary study. Burns, 12, 84-90.
36. 3+ using 1, 10-phenanthroline: III. A rapid photochemical method. Clays and Clay Minerals, 36, 379-381.
37. Lambers, H., Piessens, S., Bloem, A., Pronk, H., & Finkel, P. (2006). Natural skin surface pH is on average below 5, which is beneficial for its resident flora. International Journal of Cosmetic Science, 28, 359-370.
38. Lawrence, J. R., Swerhone, G. D. W., Leppard, G. G., Araki, T., Zhang, X., West, M. M., et al. (2003). Scanning transmission X-ray, laser scanning, and transmission electron microscopy mapping of the exopolymeric matrix of microbial biofilms. Applied and Environment Microbiology, 69, 5543-5554.
39. Lemire, J. A., Harrison, J. J., & Turner, R. J. (2013). Antimicrobial activity of metals: mechanisms, molecular targets and applications. Nature Reviews, 11, 371-384.
40. Leveen, H. H., Falk, G., Borek, B., Diaz, C., Lynfield, Y., Wynkoop, B. J., et al. (1973). Chemical acidification of wounds: An adjuvant to healing and the unfavorable action of alkalinity and ammonia. Annals of Surgery, 178, 745-753.
41. Liss, S. N., Droppo, I. G., Flannigan, D. T., & Leppard, G. G. (1996). Floc architecture in wastewater and natural riverine systems. Environmental Science and Technology, 30, 680-686.
42. Liu, Y., Kalen, A., Risto, O., & Whalstrom, O. (2002). Fibroblast proliferation due to exposure to a platelet concentrate in vitro is pH dependent. Wound Repair and Regeneration, 10, 336-340.
43. Meunier, A. (2005). Clays. Berlin, Heidelberg, New York: Springer.
44. Moore, D. M., & Reynolds, R. C. (1997). X-ray diffraction and the identification and analysis of clay minerals (2nd ed.). New York: Oxford University Press.
45. 2 in aqueous solution-basic principles and a simple heuristic description. Chemosphere, 68, 2080-2084.
46. Moses, C. O., & Herman, J. S. (1991). Pyrite oxidation at circumneutral pH. Geochimica et Cosmochimica Acta, 55, 471-482.
47. Mullen, M. D., Wolf, D. C., Ferris, F., Beveridge, T. J., Flemming, C. A., & Bailey, G. W. (1989). Bacterial sorption of heavy metals. Applied Environmental Microbiology, 55, 3143-3149.
48. Murad, E., & Rojik, P. (2004). Jarosite, schwertmannite, goethite, ferrihydrite and lepidocrocite: The legacy of coal and sulfide ore mining. Super Soil 2004: 3rd Australian New Zealand Soils Conference, Dec 2004, University of Sydney, Australia.
49. Murad, E., & Rojik, P. (2005). Iron mineralogy of mine drainage precipitates as environmental indicators: Review of the current concepts and a case study from the Sokolov Basin, Czech Republic. Clay Minerals, 40, 427-440.
50. Musk, D. J., Banko, D. A., & Hergenrother, P. J. (2005). Iron salts perturb biofilm formation and disrupt existing biofilms of Pseudomonas aeruginosa. Chemistry and Biology, 12, 789-796.
51. Nies, D. H. (1999). Microbial heavy-metal resistance. Applied Microbiology and Biotechnology, 51, 730-750.
52. Nies, D. H. (2000). Heavy metal-resistant bacteria as extremophiles: Molecular physiology and biotechnological use of Ralstonia sp. CH34. Extremophiles, 4, 77-82.
53. Nies, D. H. (2003). Efflux-mediated heavy metal resistance in prokaryotes. FEMS Microbiology Reviews, 27, 313-339.
54. Ratledge, C., & Dover, L. G. (2000). Iron metabolism in pathogenic bacteria. Annual Review of Microbiology, 54, 881-941.
55. Reynolds, R. C. (1985). NEWMOD© a computer program for the calculation of one-dimensional diffraction patterns of mixed layered clay minerals. In R. C. Reynolds, 8 Brook Rd, Hanover, New Hampshire, 03755, USA.
56. Rimstidt, J. D., & Vaughan, D. J. (2003). Pyrite oxidation: A state of the art assessment of the reaction mechanism. Geochimica et cosmochimica act, 67, 873-880.
57. Roth, R. N., & Weiss, L. D. (1994). Hyperbaric oxygen and wound healing. Clinics in Dermatology, 12, 141-156.
58. Roy, S., Khanna, S., Nallu, K., Hunt, T. K., & Sen, C. K. (2006). Dermal wound healing is subject to redox control. Molecular Therapy, 1, 211-220.
59. Schneider, L. A., Korber, A., Grabbe, S., & Dissemond, J. (2007). Influence of pH on wound-healing: A new perspective for wound therapy? Archives of Dermatological Research, 298, 413-420.
60. Schoonen, M. A. A., Harrington, A. D., Laffers, R., & Strongin, D. R. (2010). Role of hydrogen peroxide and hydroxyl radical in pyrite oxidation by molecular oxygen. Geochimica et Cosmochimica Acta, 74, 4971-4987.
61. 4 on clays between pH 5. 0 and 3. 0. Applied Geochemistry, 24, 333-345.
62. Silhavy, T. J., Kahne, D., & Walker, S. (2010). The bacterial cell envelope. Cold Spring Harbor Perspectives in Biology, 2, a000414.
63. Sillitoe, R. H., Hedenquist, J. W. (2003). Linkages between volcanotectonic settings, ore-fluid compositions, and epithermal precious metal deposits, Society of Economic Geologists, Special Publication, 10.
64. Singer, P. C., & Stumm, W. (1970). Acid mine drainage the rate determining step. University of Toronto Study, Geological Survey, 44, 83-93.
65. Smith, J. L. (2004). The physiological role of ferritin like compounds in bacteria. Clinical Reviews in Microbiology, 30, 173-185.
66. Spurr, A. R. (1969). A low-viscosity epoxy resin embedding medium for electron microscopy. Journal of Ulrastructural Research, 26, 31-43.
67. Stumm, W., & Morgan, J. J. (1996). Aquatic chemistry. Chemical equilibria and rate constants in natural waters (3rd ed.). New York: Wiley.
68. 2+-initiated lipid peroxidation in liposomes: The dual function of ferrous ions, the roles of the pre-existing lipid peroxides and the lipid peroxyl radical. Biochemical Society Journal, 352, 27-36.
69. Taylor, J. E., Laity, P. R., Hicks, J., Wong, S. S., Norris, K., Khunkamchoo, P., et al. (2005). Extent of iron pick-up in deforoxamine-coupled polyurethane materials for therapy of chronic wounds. Biomaterials, 26, 6024-6033.
70. Totsche, O., Fyson, A., Kalin, M., & Steinberg, C. E. W. (2006). Titration curves-A useful instrument for assessing the buffer systems of acidic mining waters. Environmental Science and Pollution Research, 13, 215-224.
71. Urrutia, M. M., & Beveridge, T. J. (1995). Formation of short-range ordered aluminosilicates in the presence of a bacterial surface (Bacillus subtilis) and organic ligands. Geoderma, 65, 149-165.
72. Valverde, A., Delvasto, P., Peix, A., Velazquez, E., Santa-Regina, I., Ballester, A., et al. (2006). Burkholderia ferrariae sp. Nov., isolated from an iron ore in Brazil. International Journal of Systematic and Evolutionary Microbiology, 56, 2421-2425.
73. Weller, R., & Finnen, M. J. (2006). The effects of topical treatment with acidified nitrite on wound healing in normal and diabetic mice. Nitric Oxide, 15, 395-399.
74. Weller, R., Price, R. J., Ormerod, A. D., Benjamin, N., & Leifert, C. (2001). Antimicrobial effect of acidified nitrite on dermatophyte fungi. Candida and bacterial skin pathogens. Journal of Applied Microbiology, 90, 648-652.
75. Williams, R. J. P. (1999). What is wrong with aluminium? The J. D. Birchall memorial lecture. Journal of Inorganic Biochemistry, 76, 81-88.
76. Williams, L. B., & Haydel, S. E. (2010). Evaluation of the medicinal use of clay minerals as antibacterial agents. International Geology Review, 52(7-8), 745-770.
77. Williams, L. B., Haydel, S. E., Giese, R. F., & Eberl, D. D. (2008). Chemical and mineralogical characteristics of French green clays used for healing. Clays and Clay Minerals, 56, 437-452.
78. Williams, L. B., Holland, M., Eberl, D. D., Brunet, T., & Brunet de Courrsou, L. (2004). Killer clays! Natural antibacterial clay minerals. Mineralogical Society Bulletin, 139, 3-8.
79. Williams, L. B., Metge, D. W., Eberl, D. D., Harvey, R. W., Turner, A. G., Prapaipong, P., et al. (2011). What makes a natural clay antibacterial? Environmental Science and Technology, 45, 3768-3773.
80. Wilson, E., Henry, D. A., & Smith, J. A. (1990). Disk elution method for MICs and MBCs. Antimicrobial Agents and Chemotherapy, 34, 2128-2132.
81. Yariv, S. (1992). The effect of tetrahedral substitution of Si by Al on the surface acidity of the oxygen plane of clay minerals. International Reviews in Physical Chemistry, 11, 345-375.
82. Yariv, S., & Cross, H. (2002). Organo-clay complexes and interactions (pp. 1-38). New York: Marcel Dekker, Inc.