Hostname: page-component-586b7cd67f-tf8b9 Total loading time: 0 Render date: 2024-11-22T23:44:50.199Z Has data issue: false hasContentIssue false
  • English
  • Français

Geomimicry: harnessing the antibacterial action of clays

Published online by Cambridge University Press:  02 January 2018

Lynda B. Williams
Lynda B. Williams*
Affiliation:
School of Earth & Space Exploration, Arizona State University, Tempe, AZ 85287-1404, USA
*
†E-mail: [email protected]
Rights & Permissions [Opens in a new window]

Abstract

Core share and HTML view are not available for this content. However, as you have access to this content, a full PDF is available via the ‘Save PDF’ action button.

A decade of research on clays that kill human pathogens, including antibiotic-resistant strains such as methicillin-resistant S. aureus (MRSA), has documented their common characteristics. Worldwide, ∼5% of clays tested to date are antibacterial when hydrated. Most antibacterial clays are from hydrothermally altered volcanics, where volcanogenic fluids produce minerals containing reduced metals. Ferruginous illite-smectite (I-S) is the most common clay mineral, although kaolins dominate some samples. Antibacterial clay mineral assemblages may contain other reduced Fe minerals (e.g. pyrite) that drive production of reactive oxygen species (H2O2, •OH, •O2−) and cause damage to cell membranes and intracellular proteins. Ion exchange can also cause loss of bacterial membrane-bound Ca2+, Mg2+ and PO43–.

Critically important is the role of clays in buffering the hydration water pH to conditions where Al and Fe are soluble. A nanometric particle size (<200 nm) is characteristic of antibacterial clays and may be a feature that promotes dissolution. Clay interlayers or the lumen of tubular clays may absorb reduced transition metals, protecting them from oxidation. When the clays are mixed with deionized water for medicinal applications, these metals are released and oxidized.

Different antibacterial clays exhibit different modes of action. The minerals may be a source of toxins, or by adsorption may deprive bacteria of essential nutrients. In the field, the pH and Eh (oxidation state) of the hydrated clay may help to identify potential antibacterial clays. If the pH is circum-neutral, toxic metals are not soluble. However, at pH < 5 or >9 many metals are soluble and the oxidation of transition metals increases the Eh of the suspension to >400 mV, leading to bacterial oxidation.

Understanding the antibacterial mechanism of natural clay may lead to design of new treatments for antibiotic-resistant bacteria, with potential applications in wound dressings, medical implants ( joint replacements, catheters), animal feed stocks, agricultural pathogens, and production of antibacterial building materials. This research exemplifies how ‘geomimicry’ (copying geochemical processes) may open new frontiers in science.

Keywords

geomimicryantibacterial clayantibiotic resistancehydrothermalmetal oxidation
Type
Research Article
Information
Clay Minerals , Volume 52 , Issue 1 , March 2017 , pp. 1 - 24
Creative Commons
Creative Common License - CCCreative Common License - BY
Copyright © The Mineralogical Society of Great Britain and Ireland 2017 This is an Open Access article, distributed under the terms of the Creative Commons Attribution license. (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted re-use, distribution, and reproduction in any medium, provided the original work is properly cited.
Copyright
Copyright © The Mineralogical Society of Great Britain and Ireland 2017

References

Amyes, S., Miles, R.S., Thomson, C.J. & Tillotson, G. (1996) Antimicrobial Chemotherapy. CRC Press, Taylor & Francis Group, Boca Raton, Florida, USA, 72 pp.Google Scholar
Andrews, S.C., Robinson, A.K. & Francisco, R.-Q. (2003) Bacterial iron homeostasis. FEMS Microbiology Reviews, 27, 215–237.CrossRefGoogle ScholarPubMed
Bacon, C.R. & Nathenson, M. (1996) Geothermal resources in the Crater Lake area, Oregon. U.S. Geological Survey Open-File Report, 96-663.CrossRefGoogle Scholar
Baker, S.E., Sawvel, A.M., Zheng, N. & Stucky, G.D. (2007) Controlling bioprocesses with inorganic surfaces: Layered clay hemostatic agents. Chemistry of Materials, 19, 4390–439.CrossRefGoogle Scholar
Barbusinski, K. (2009) Fenton reaction: Controversy concerning the chemistry. Ecological Chemistry and Engineering, 16, 347–358.Google Scholar
Bauer, A.W., Kirby, W.M.M., Sherris, J.C. & Turck, M. (1966) Antibiotic susceptibility testing by a standar-dized single disk method. American Journal of Clinical Pathology, 45, 493–496.CrossRefGoogle Scholar
Carretero, M.L., Gomes, C.S.F. & Tateo, F. (2013) Clays and human health. Pp. 717–741 in: Handbook of Clay Science, 2nd edition (F. Bergaya & G. Lagaly, editors). Developments in Clay Science 5, Elsevier, Amsterdam.Google Scholar
CLSI, Clinical Laboratory Standards Institute (2015) Methods for Dilution Antimicrobial Susceptibility Tests for Bacteria That Grow Aerobically; Approved Standard — tenth edition. Wayne, Pennsylvania, USA, CLSI document M07-A10, 35, pp. 1–5.Google Scholar
Cohn, C.A., Pak, A., Strongin, D. & Schoonen, M.A. (2005) Quantifying hydrogen peroxide in iron containing solutions using leuco-crystal violet. Geochemical Transactions, 6, 47–51.CrossRefGoogle ScholarPubMed
Eberl, D.D. (2003) User's guide to RockJock; A program for determining quantitative mineralogy from powder X-ray diffraction data. U.S. Geological Survey Open-File Rep. 2003-78, 47 pp.CrossRefGoogle Scholar
Fenton, H.J.H. (1894) Oxidation of tartaric acid in presence of iron. Journal of Chemical Society Transactions, 65, 899–911.CrossRefGoogle Scholar
Ferrell, R.E. Jr. (2008) Medicinal clay and spiritual healing. Clays and Clay Minerals, 56, 751–760.CrossRefGoogle Scholar
Foster, J.W. and Woodruff, H.B. (2010) Antibiotic substances produced by bacteria. Annals of the New York Academy of Science, 2013, 125–136.CrossRefGoogle Scholar
Friedlander, L.R., Puri, N., Schoonen, M.A.A. & Karzai, W. (2015) The effect of pyrite on Escherichia coli in water: proof-of-concept for the elimination of water-borne bacteria by reactive minerals. Journal of Water Health, 13, 1, 42–53.Google ScholarPubMed
George, K.M., Chatterjee, D., Gunawardana, G., Welty, D., Hayman, J., Lee, R. & Small, P.L.C. (1999) Mycolactone: a polyketide toxin from Mycobacterium ulcerans required for virulence. Science, 283, 854–7.CrossRefGoogle ScholarPubMed
Guida, L., Saidi, Z., Hughes, M. & Poole, R. (1991) Aluminum toxicity and binding t. Escherichia coli. Archives of Microbiology, 156, 507–512.Google Scholar
Gutteridge, J.M., Quinlan, G.J., Clark, I. & Halliwell, B. (1985) Aluminium salts accelerate peroxidation of membrane lipids stimulated by iron salts. Biochimica et Biophysica Acta — Lipids and Lipid Metabolism, 835, 441–447.CrossRefGoogle ScholarPubMed
Haydel, S.E., Remenih, C.M. & Williams, L.B. (2008) Broad-spectrum in vitro antibacterial activities of clay minerals against antibiotic-susceptible and antibiotic-resistant bacterial pathogens. Journal of Antimicrobial Chemotherapy, 61, 353–361.CrossRefGoogle ScholarPubMed
Hoogerheide, J.C. (1944) Antibiotic substances produced by soil bacteria. Botanical Review, 10, 599–638.CrossRefGoogle Scholar
Hoorn, C. (1994) Fluvial palaeoenvironments in the intracratonic Amazonas Basin (early Miocene-early Middle Miocene, Colombia). Palaeogeography & Palaeoclimate, 109, 1–54.CrossRefGoogle Scholar
Hyslop, P.A., Hinshaw, D.B., Scraufstatter, I.U., Cochrane, C.G., Kunz, S. & Vosbeck, K. (1995) Hydrogen peroxide as a potent bacteriostatic antibiotic: implications for host defense. Free Radical Biology and Medicine, 19, 31–37.CrossRefGoogle ScholarPubMed
Kammler, M., Schön, C. & Hantke, K. (1993) Characterization of the ferrous iron uptake system o. Escherichia coli. Journal of Bacteriology, 175, 6212–621.Google Scholar
Keyer, K. & Imlay, J.A. (1996) Superoxide accelerates DNA-damage by elevating free-iron levels. Proceedings of the National Academy of Sciences, USA, 193, 13635–1363.CrossRefGoogle Scholar
Kibanova, D., Nieto-Camacho, A. & Cervini-Silva, J. (2009) Lipid peroxidation induced by expandable clay minerals. Environmental Science & Technology, 43, 7550–755.CrossRefGoogle ScholarPubMed
King, G.M., Weber, C.F., Ohta, H., Sato Y & Nanba, K. (2008) Molecular survey and activities of carbon monoxide oxidizing bacteria on volcanic deposits in Miyake-jima, Japan. Microbes & Environments, 23, 299–305.CrossRefGoogle Scholar
Konhauser, K.O. & Urrutia, M.M. (1999) Bacterial clay authigenesis: a common biogeochemical process. Chemical Geology, 161, 399–413.CrossRefGoogle Scholar
Kvitko, B.H., Goodyear, A., Propst, K.L., Dow, S.W. & Schweizer, H.P. (2012) Burkholderia pseudomallei known siderophores and Hemin uptake are dispensable for lethal Murine Melioidosis. Public Library of Science: Neglected Tropical Diseases, 6, e1715.Google Scholar
Lawton, G., Granville-Chapman, J. & Parker, P.J. (2009) Novel hemostatic dressings. Journal of the Royal Army Medical Corps, 155, 309–314.CrossRefGoogle Scholar
Lemire, J.A., Harrison, J.J. & Turner, R.J. (2013) Antimicrobial activity of metals: mechanisms, molecular targets and applications. Nature Reviews 11, 371–384.Google ScholarPubMed
Londoño, S.C. & Williams, L.B. (2016) Unraveling the antibacterial mode of action of a clay from the Colombian Amazon. Environmental Geochemistry & Health, 38, 363–379.CrossRefGoogle ScholarPubMed
Londoño, S.C., Hartnett, H.H. & Williams, L.B. (2017) The antibacterial activity of aluminum in clay from the Colombian Amazon. Environmental Science & Technology. doi: 10.1021/acs.est.6b04670.CrossRefGoogle Scholar
Marsollier, L., Rober, R., Aubry, J., Saint André, J.-P., Kouakou, H., Legras, P., Manceau, A.-L., Mahaza C & Carbonnelle, B. (2002) Aquatic insects as a vector for Mycobacterium ulcerans. Applied & Environmental Microbiology, 68, 4623–462.CrossRefGoogle ScholarPubMed
Moore, D.M. & Reynolds, R.C. (1997) X-ray Diffraction and the Identification and Analysis of Clay Minerals, 2nd edition. Oxford University Press, New York.Google Scholar
Morrison, K.D. (2015) Unearthing the antibacterial activity of a natural clay deposit. PhD dissertation, Arizona State University, Arizona, USA, 157 pp.Google Scholar
Morrison, K.D., Underwood, J.C., Metge, D.W., Eberl, D.D. & Williams, L.B. (2014) Mineralogical variables that control the antibacterial effectiveness of a natural clay deposit. Environmental Geochemistry & Health, 36, 613–631.CrossRefGoogle ScholarPubMed
Morrison, K.D., Misra, R. & Williams, L.B. (2016) Unearthing the antibacterial mechanism of medicinal clay: A geochemical approach to combating antibiotic resistance. Nature Scientific Reports, 5, 19043; doi: 10.1038/srep19043.Google Scholar
Nies, D.H. (1999) Microbial heavy-metal resistance. Applied Microbiology & Biotechnology, 51, 730–750.CrossRefGoogle ScholarPubMed
Orphan, V.J. & House, C.H. (2009) Geobiological investigations using secondary ion mass spectrometry: microanalysis of extant and paleo-microbial processes. Geobiology, 7, 360–372.CrossRefGoogle ScholarPubMed
Portaels, F., Meyers, W.M., Ablordey, A., Castro, A.G., Chemlal, K. (2008) First cultivation and characterization of Mycobacterium ulcerans from the environment. Public Library of Science Neglected Tropical Diseases 2, e178. doi: 10.1371/journal.pntd.0000178.Google ScholarPubMed
Prousek, J. (2007) Fenton chemistry in biology and medicine. Pure & Applied Chemistry, 79, 2325–2338.CrossRefGoogle Scholar
Repine, J.E., Fox, R.B. & Berger, E.M. (1981) Hydrogen peroxide kills Staphylococcus aureus by reacting with Staphylococcal iron to form hydroxyl radicals. Journal of Biological Chemistry, 256, 7094–7096.CrossRefGoogle Scholar
Rimstidt, J.D. & Vaughan, D.J. (2003) Pyrite oxidation: A state-of-the-art assessment of the reaction mechanism. Geochimica et Cosmochimica Acta, 67, 873–880.CrossRefGoogle Scholar
Schmidt, D., Jiang, Q. & McKinnon, R. (2006) Phospholipids and the origin of cationic gating charges in voltage sensors. Nature, 444, 775–779.CrossRefGoogle ScholarPubMed
Schoonen, M.A.A., Harrington, A.D., Laffers, R. and Strongin, D.R. (2010) Role of hydrogen peroxide and hydroxyl radical in pyrite oxidation by molecular oxygen. Geochimica et Cosmochimica Acta, 74, 4971–4987.CrossRefGoogle Scholar
Takeno, N. (2005) Atlas of Eh-pH diagrams: Intercomparison of thermodynamic databases. Geological Survey of Japan Open File Report No. 419,285 pp.Google Scholar
Vermeer, D.E. & Ferrell, R.E. Jr. (1985) Nigerian geophagical clay: A traditional antidiarrheal pharmaceutical. Science, 227, 634–636.CrossRefGoogle Scholar
Weber, C.F. & King, G.M. (2010) Quantification of Burkholderia coxL genes in Hawaiian volcanic deposits. Applied Environmental Microbiology, 76, 2212–2217.CrossRefGoogle ScholarPubMed
Wei, J.-C., Yen, Y.-T., Su, H.-L. & Lin, J.-J. (2011) Inhibition of bacterial growth by the exfoliated clays and observation of physical capturing mechanism.. The Journal of Physical Chemistry C, 115, 18770–18775.CrossRefGoogle Scholar
WHO, World Health Organization (2008) Buruli ulcer disease (Mycobacterium ulcerans infection). World Health Organization. http://www.who.int/mediacentre/factsheets/fs199/en/ Google Scholar
Williams, R.J.P. (1999) What is wrong with aluminum. Journal of Inorganic Biochemistry, 76, 81–88.CrossRefGoogle Scholar
Williams, L.B. & Haydel, S.E. (2010) Evaluation of the medicinal use of clay minerals as antibacterial agents. International Geology Review, 52, 745–770.CrossRefGoogle ScholarPubMed
Williams, L.B. & Hillier, S. (2014) Kaolins and health: from first grade to first aid. Elements, 10, 207–211.CrossRefGoogle Scholar
Williams, L.B., Holland, M., Eberl, D.D., Brunet, T. & Brunet de Courssou, L. (2004) Killer clays! Natural antibacterial clay minerals.. Mineralogical Society Bulletin, 139, 3–8.Google Scholar
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, 437–52.CrossRefGoogle ScholarPubMed
Williams, L.B., Metge, D.W., Eberl, D.D., Harvey, R.W., Turner, A.G., Prapaipong, P. & Poret-Peterson, A.T. (2011) What makes natural clays antibacterial. Environmental Science & Technology, 45, 3768–3773.CrossRefGoogle ScholarPubMed
Wilson, M.J. (2003) Clay mineralogical and related characteristics of geophagic materials.. Journal of Chemical Ecology, 29, 1525–1547.CrossRefGoogle ScholarPubMed
Wilson, R.G., Stevie, F.A. & Magee, C.W. (1989) Secondary Ion Mass Spectrometry: A Practical Handbook for Depth Profiling and Bulk Impurity Analysis. Wiley Interscience Publishers, New York, 384 pp.Google Scholar
Winterbourn, C.C. (2008) Reconciling the chemistry and biology of reactive oxygen species. Natural Chemical Biology, 4, 278–286.CrossRefGoogle ScholarPubMed
Yokoyama, S., Kuroda, M. & Sato, T. (2005) Atomic force microscopy study of montmorillonite dissolution under highly alkaline conditions.. Clays and Clay Minerals, 53, 147–154.CrossRefGoogle Scholar
Young, S.L. (2011) Craving Earth. Columbia University Press, New York, 228 pp.CrossRefGoogle ScholarPubMed
Zatta, P., Kiss, T., Suwalsky, M. & Berthon, G. (2002) Aluminium (III) as a promoter of cellular oxidation. Coordination Chemistry Reviews, 228, 271–284.CrossRefGoogle Scholar
Zeelmaekers, E., McCarty, D. & Mystkowski, K. (2009) Sybilla User Manual, Chevron ®ETC proprietary software. 16 pp.Google Scholar