Microbe-mineral interactions: The impact of surface attachment on mineral weathering and element selectivity by microorganisms

Chemical Geology

Volumn 403, Issue , 2015, Pages 13-23

  Ahmed, Engy ^a   Holmström, Sara J M ^a  

^a STOCKHOLM UNIVERSITY   (Sweden)

Author keywords

Acidification; Bacteria; Biotite; Complexation; Fungi; Siderophores

Indexed keywords

ACIDIFICATION; BIOMINERALIZATION; BIOREMEDIATION; BIOTITE; COMPLEXATION; DISSOLUTION; FUNGI; MICA; SOILS; WEATHERING;

COMPLEXATION PROCESS; ELEMENT COMPOSITIONS; MINERAL DISSOLUTION; MINERAL INTERACTIONS; PSEUDOMONAS MENDOCINA; PSEUDOMONAS STUTZERI; SIDEROPHORES; SURFACE ATTACHMENT;

BACTERIA;

ACIDIFICATION; BACTERIUM; BIOTITE; CHEMICAL WEATHERING; COMPLEXATION; FUNGUS; MICROBIAL ACTIVITY; SIDEROPHORE;

BACTERIA (MICROORGANISMS); ERWINIA AMYLOVORA; FUNGI; NEUROSPORA CRASSA; PENICILLIUM MELINII; PSEUDOMONAS MENDOCINA; PSEUDOMONAS STUTZERI; STREPTOMYCES PILOSUS;

EID: 84928339379     PISSN: 00092541     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.chemgeo.2015.03.009     Document Type: Article

References (97)

1. Absolom D.R., Lamberti F.V., Policova A., Zingg W., VanOss C.J., Neumann A.W. Surface thermodynamics of bacterial adhesion. Appl. Environ. Microbiol. 1983, 46:90-97.
2. Acker J.G., Bricker O.P. The influence of pH on biotite dissolution and alteration kinetics at low temperature. Geochim. Cosmochim. Acta 1992, 56:3073-3092. 10.1016/0016-7037(92)90290-Y.
3. Ahmed E., Holmström S.J.M. Siderophores in environmental research: roles and applications. Microb. Biotechnol. 2014, 7:196-208. 10.1111/1751-7915.12117.
4. Ahmed E., Holmström S.J.M. Siderophore production by microorganisms isolated from a podzol soil profile. Geomicrobiol J. 2015, (in press). 10.1080/01490451.2014.925011.
5. Ahmed E., Holmström S.J.M. The effect of soil horizon and mineral type on the distribution of siderophores in soil. Geochim. Cosmochim. Acta 2014, 131:184-195. 10.1016/j.gca.2014.01.031.
6. Annachhatre A.P., Bhamidimarri S.M.R. Microbial attachment and growth in fixed-film reactors: process startup considerations. Biotechnol. Adv. 1992, 10:69-91. 10.1016/0734-9750(92)91352-F.
7. Balland C., Poszwa A., Leyval C., Mustin C. Dissolution rates of phyllosilicates as a function of bacterial metabolic diversity. Geochim. Cosmochim. Acta 2010, 74:5478-5493. 10.1016/j.gca.2010.06.022.
8. Balland-Bolou-Bi C., Poszwa A., Mustin C. Experimental study on the phlogopite weathering potential of bacterial communities isolated from different soil profiles. Am. Int. J. Biol. 2014, 2:35-63. 10.15640/aijb.v2n3-4a3.
9. Balogh-Brunstad Z., Keller C.K., Gill R.A., Bormann B.T., Li C.Y. The effect of bacteria and fungi on chemical weathering and chemical denudation fluxes in pine growth experiments. Biogeochemistry 2008, 88:153-167. 10.1007/s10533-008-9202-y.
10. Banfield J.F., Barker W.W., Welch S.A., Taunton A. Biological impact on mineral dissolution: application of the lichen model to understanding mineral weathering in the rhizosphere. Proc. Natl. Acad. Sci. U. S. A. 1999, 96:3404-3411. 10.1073/pnas.96.7.3404.
11. Bennett P.C., Hiebert F.K., Choi W.J. Microbial colonization and weathering of silicates in a petroleum-contaminated groundwater. Chem. Geol. 1996, 132:45-53. 10.1016/S0009-2541(96)00040-X.
12. Bennett P.C., Rogers J.R., Choi W.J., Hiebert F.K. Silicates, silicate weathering, and microbial ecology. Geomicrobiol J. 2001, 18:3-19. 10.1080/01490450151079734.
13. Berner R.A., Berner E.K. Silicate weathering and climate. Tectonic Uplift and Climate Change 1997, 353-365. Springer, New York. 10.1007/978-1-4615-5935-1_15. W.F. Ruddiman (Ed.).
14. 2 over phanerozoic time. Am. J. Sci. 2001, 301:182-204. 10.2475/ajs.301.2.182.
15. Berner R.A., Lasaga A.C., Garrels R.M. The carbonate-silicate geochemical cycle and its effect on atmospheric carbon dioxide over the past 100millionyears. Am. J. Sci. 1983, 283:641-683. 10.2475/ajs.283.7.641.
16. Beveridge T.J., Makin S.A., Kadurugamuwa J.L., Li Z. Interactions between biofilms and the environment. FEMS Microbiol. Rev. 1997, 20:291-303. 10.1016/S0168-6445(97)00012-0.
17. Bonneville S., Smits M.M., Brown A., Harrington J., Leake J.R., Brydson R., Benning L.G. Plant-driven fungal weathering: early stages of mineral alteration at the nanometer scale. Geology 2009, 37:615-618. 10.1130/G25699A.1.
18. Bonneville S., Morgan D.J., Schmalenberger A., Bray A., Brown A., Banwart S.A., Benning L.G. Tree-mycorrhiza symbiosis accelerate mineral weathering: evidences from nanometer-scale elemental fluxes at the hypha-mineral interface. Geochim. Cosmochim. Acta 2011, 75:6988-7005. 10.1016/j.gca.2011.08.041.
19. Bray A.W. Mineral Weathering and Soil Formation: The Role of Microorganisms 2014, (PhD Thesis), The University of Leeds.
20. Brisou J.F. Biofilms: Methods for Enzymatic Release of Microorganisms 1995, CRC Press, Boca Raton.
21. Brown C.M. Growth of bacteria at surfaces: influence of nutrient limitation. FEMS Microbiol. Lett. 1977, 1:163-166.
22. Brown G.E., Foster A.L., Ostergren J.D. Mineral surfaces and bioavailability of heavy metals: a molecular-scale perspective. Proc. Natl. Acad. Sci. U. S. A. 1999, 96:3388-3395. 10.1073/pnas.96.7.3388.
23. Buss H.L. Biogeochemical Weathering of Iron-silicate Minerals 2006, PhD Thesis, The Pennsylvania State University.
24. Buss H.L., Lüttge A., Brantley S.L. Etch pit formation on iron silicate surfaces during siderophore-promoted dissolution. Chem. Geol. 2007, 240:326-342. 10.1016/j.chemgeo.2007.03.003.
25. Buss H.L., Sak P.B., Webb S.M., Brantley S.L. Weathering of the Rio Blanco quartz diorite, Luquillo Mountains, Puerto Rico: coupling oxidation, dissolution, and fracturing. Geochim. Cosmochim. Acta 2008, 72:4488-4507. 10.1016/j.gca.2008.06.020.
26. Calvaruso C., Turpault M.P., Frey-Klett P. Root-associated bacteria contribute to mineral weathering and to mineral nutrition in trees: a budgeting analysis. Appl. Environ. Microbiol. 2006, 72:1258-1266. 10.1128/AEM. 72.2.1258-1266.2006.
27. Calvaruso C., Turpault M., Leclerc E., Ranger J., Garbaye J., Uroz S., Frey-Klett P. Influence of forest trees on the distribution of mineral weathering-associated bacterial communities of the Scleroderma citrinum mycorrhizosphere. Appl. Environ. Microbiol. 2010, 76:4780-4787. 10.1128/AEM.03040-09.
28. Cheah S.F., Kraemer S.M., Cervini-Silva J., Sposito G. Steady-state dissolution kinetics of goethite in the presence of desferrioxamine B and oxalate ligands: implications for the microbial acquisition of iron. Chem. Geol. 2003, 198:63-75. 10.1016/S0009-2541(02)00421-7.
29. Cowan M.M., Warren T.M., Fletcher M. Mixed-species colonization of solid surfaces in laboratory biofilms. Biofouling 1991, 3:23-34. 10.1080/08927019109378159.
30. Dong H. Mineral-microbe interactions: a review. Front Earth Sci. Chin. 2010, 4:127-147. 10.1007/s11707-010-0022-8.
31. Donlan R.M. Biofilms: microbial life on surfaces. Emerg. Infect. Dis. 2002, 8:881-890. 10.3201/eid0809.020063.
32. Drever J.I., Hurcomb D.R. Neutralization of atmospheric acidity by chemical weathering in an alpine drainage basin in the North Cascade Mountains. Geology 1986, 14:221-224. 10.1130/0091-7613(1986)14<221:NOAABC>2.0.CO;2.
33. Duckworth O.W., Akafia M.M., Andrews M.Y., Bargar J.R. Siderophore-promoted dissolution of chromium from hydroxide minerals. Environ. Sci.: Processes Impacts 2014, 16:1348-1359. 10.1039/C3EM00717K.
34. Dutton M.V., Evans C.S. Oxalate production by fungi: its role in pathogenicity and ecology in the soil environment. Can. J. Microbiol. 1996, 42:881-895. 10.1139/m96-114.
35. Fein J.B., Boily J., Yee N., Gorman-Lewis D., Turner B.F. Potentiometric titrations of Bacillus subtilis cells to low pH and a comparison of modeling approaches. Geochim. Cosmochim. Acta 2005, 69:1123-1132. 10.1016/j.gca.2004.07.033.
36. Fletcher M. The applications of interference reflection microscopy to the study of bacterial adhesion to solid surfaces. Biodeterioration 1988, 7:31-35. Elsevier Applied Science, London. D.R. Houghton, R.N. Smith, H.O.W. Eggins (Eds.).
37. Fletcher M. Attachment of Pseudomonas fluorescens to glass and influence of electrolytes on bacterium-substratum separation distance. J. Bacteriol. 1998, 170:2027-2030.
38. Fowle D.A., Kulczycki E., Roberts J.A. Linking bacteria-metal interactions to mineral attachment: a role for outer sphere complexation of cations?. Proceedings of the Eleventh International Symposium on Water-Rock Interaction WRI-11, Saratoga Springs, NY, USA 2004, 2:1113-1117. R.B. Wanty (Ed.).
39. 3+. Geochim. Cosmochim. Acta 2008, 72:3381-3397. 10.1016/j.gca.2008.03.027.
40. Hameeda B., Reddy Y.H., Rupela O.P., Kumar G.N., Reddy G. Effect of carbon substrates on rock phosphate solubilization by bacteria from composts and macrofauna. Curr. Microbiol. 2006, 53:298-302. 10.1007/s00284-006-0004-y.
41. Hider R.C., Kong X. Chemistry and biology of siderophores. Nat. Prod. Rep. 2010, 27:637-657. 10.1039/b906679a.
42. Hoffland E., Kuyper T.W., Wallander H., Plassard C., Gorbushina A.A., Haselwandter K., Holmström S., Landeweert R., Lundström U.S., Rosling A., Sen R., Smits M.M., van Hees P., van Breemen N. The role of fungi in weathering. Front. Ecol. Environ. 2004, 2:258-264. 10.1890/1540-9295(2004)002[0258:TROFIW]2.0.CO;2.
43. Holland S.P. Characterizing Clay-Microbe-Metal Interactions: Implications for Metal Immobilization 2011, McMaster University, Master Thesis.
44. Hopf J., Langenhorst F., Pollok K., Merten D., Kothe E. Influence of microorganisms on biotite dissolution: an experimental approach. Chem. Erde 2009, 69:45-56. 10.1016/j.chemer.2008.11.001.
45. Huntington T.G., Hooper R.P., Johnson C.E., Aulenbach B.T., Cappellato R., Blum A.E. Calcium depletion in forest ecosystems of the southeastern United States Forest Ecosystem. Soil Sci. Soc. Am. J. 2000, 64:1845-1858. 10.2136/sssaj2000.6451845x.
46. Hutchens E. Microbial selectivity on mineral surfaces, possible implications for weathering processes. Fungal Biol. Rev. 2009, 23:115-121. 10.1016/j.fbr.2009.10.002.
47. 4 with P-solubilizing microorganism. Soil Biol. Biochem. 1995, 27:265-270. 10.1016/0038-0717(94)00205-F.
48. Jalal M.A.F., van der Helm D. Identification isolation and spectroscopic of fungal siderophores. Handbook of Microbial Iron Chelates 1991, 235-270. CRC Press Inc., Boca Raton FL. G. Winkelmann (Ed.).
49. Johnston C.G., Vestal J.R. Biogeochemistry of oxalate in the Antarctic cryptoendolithic lichen dominated community. Microb. Ecol. 1993, 25:305-319. 10.1007/BF00171895.
50. Jones A.A., Bennett P.C. Mineral microniches control the diversity of subsurface microbial populations. Geomicrobiol J. 2014, 31:246-261. 10.1080/01490451.2013.809174.
51. Kalinowski B.E., Schweda P. Kinetics of muscovite, phlogopite, and biotite dissolution and alteration at pH1-4, room temperature. Geochim. Cosmochim. Acta 1996, 60:367-385. 10.1016/0016-7037(95)00411-4.
52. Kalinowski B.E., Liermann L.J., Givens S., Brantley S.L. Rates of bacteria-promoted solubilization of Fe from minerals: a review of problems and approaches. Chem. Geol. 2000, 169:357-370. 10.1016/S0009-2541(00)00214-X.
53. Kefford B., Marshall K.C. Adhesion of Leptospira at a solid-liquid interface - a model. Arch. Microbiol. 1984, 138:84-88. 10.1007/BF00425413.
54. Kjelleberg S., Marshall K.C., Hermansson M. Oligotrophic and copiotrophic marine bacteria - observations related to attachment. FEMS Microbiol. Ecol. 1985, 31:89-96. 10.1111/j.1574-6968.1985.tb01135.x.
55. Landeweert R., Hoffland E., Finlay R.D., Kuyper T.W., van Breemen N. Linking plants to rocks: ectomycorrhizal fungi mobilize nutrients from minerals. Trends Ecol. Evol. 2001, 16:248-254. 10.1016/S0169-5347(01)02122-X.
56. Lehman R.M., Roberto F.F., Earley D., Bruhn D.F., Brink S.E., O'Connell S.P., Delwiche M.E., Colwell F.S. Attached and unattached bacterial communities in a 120-meter corehole in an acidic, crystalline rock aquifer. Appl. Environ. Microbiol. 2001, 67:2095-2106. 10.1128/AEM. 67.5.2095-2106.2001.
57. Li J., Zhang W., Li S., Li X., Lu J. Effects of citrate on the dissolution and transformation of biotite, analyzed by chemical and atomic force microscopy. Appl. Geochem. 2014, 51:101-108. 10.1016/j.apgeochem.2014.10.001.
58. Liermann L.J., Barnes A.S., Kalinowski B.E., Zhou X., Brantley S.L. Microenvironments of pH in biofilms grown on dissolving silicate surfaces. Chem. Geol. 2000, 171:1-16. 10.1016/S0009-2541(00)00202-3.
59. Liermann L.J., Kalinowski B.E., Brantley S.L., Ferry J.G. Role of bacterial siderophores in dissolution of hornblende. Geochim. Cosmochim. Acta 2000, 64:587-602. 10.1016/S0016-7037(99)00288-4.
60. Lin T.F., Huang H.I., Shen F.T., Young C.C. The protons of gluconic acid are the major factor responsible for the dissolution of tricalcium phosphate by Burkholderia cepacia CC-A174. Bioresour. Technol. 2006, 97:957-960. 10.1016/j.biortech.2005.02.017.
61. Little B.J., Wagner P.A., Lewandowski Z. Spatial relationships between bacteria and mineral surfaces. Geomicrobiology: Interactions Between Microbes and Minerals, Reviews in Mineralogy 1997, Vol. 35:123-159. Mineralogical Society of America, Washington, DC. J.F. Banfield, K.H. Nealson (Eds.).
62. Madigan M.T., Martinko J.M., Parker J. Brock Biology of Microorganisms 2000, Prentice Hall.
63. Malmström M., Banwart S. Biotite dissolution at 25°C: the pH dependence of dissolution rate and stoichiometry. Geochim. Cosmochim. Acta 1997, 61:2779-2799. 10.1016/S0016-7037(97)00093-8.
64. Marshall K.C. Planktonic versus sessile life of prokaryotes. The Prokaryotes: A Handbook on the Biology of Bacteria: Ecophysiology, Isolation, Identification, Applications 1992, 262-275. Springer-Verlag, New York. 2nd ed. A. Balows, H.G. Truper, M. Dworkin, W. Harder, K.-H. Schleifer (Eds.).
65. Matzanke B.F. Structures, coordination chemistry and functions of microbial iron chelates. CRC Handbook of Microbial Iron Chelates 1991, 15-64. CRC Press, Boca Raton, FL, USA. G. Winkelmann (Ed.).
66. Meychik N.R., Yermakov I.P. A new approach to the investigation on the tonogenic groups of root cell walls. Plant Soil 1999, 217:257-264. 10.1023/A:1004675309128.
67. Meychik N.R., Yermakov I.P. Ion exchange properties of plant root cell walls. Plant Soil 2001, 234:181-193. 10.1023/A:1017936318435.
68. Mills A.L. Keeping in touch: microbial life on soil particle surfaces. Adv. Agron. 2003, 78:1-43. 10.1016/S0065-2113(02)78001-2.
69. Miot J., Benzerara K., Kappler A. Investigating microbe-mineral interactions: recent advances in X-ray and electron microscopy and redox-sensitive methods. Annu. Rev. Earth Planet. Sci. 2014, 42:271-289. 10.1146/annurev-earth-050212-124110.
70. Murakami T., Utsunomiya S., Yokoyama T., Kasama T. Biotite dissolution processes and mechanisms in the laboratory and in nature: early stage weathering environment and vermiculitization. Am. Mineral. 2003, 88:377-386.
71. Nautiyal C.S., Bhadauria S., Kumar P., Lal H., Mondal R., Verma D. Stress induced phosphate solubilization in bacteria isolated from alkaline soils. FEMS Microbiol. Lett. 2000, 182:291-296. 10.1016/S0378-1097(99)00605-9.
72. Ojeda L., Keller G., Mühlenhoff U., Rutherford J.C., Lill R., Winge D. Role of glutaredoxin-3 and glutaredoxin-4 in the iron regulation of the Aft1 transcriptional activator in Saccharomyces cerevisiae. J. Biol. Chem. 2006, 281:17661-17669. 10.1074/jbc.M602165200.
73. Perrin D.D. Stability Constants: Part B 1979, IUPAC, Pergamon, Turkey.
74. Phillips-Lander C.M., Fowle D.A., Taunton A., Hernandez W., Mora M., Moore D., Shinogle H., Roberts J.A. Silicate dissolution in Las Pailas Thermal Field: implications for microbial weathering in acidic volcanic hydrothermal spring systems. Geomicrobiol J. 2014, 31:23-41. 10.1080/01490451.2013.802395.
75. Reichard P.U., Kretzschmar R., Kraemer S.M. Dissolution mechanisms of goethite in the presence of siderophores and organic acids. Geochim. Cosmochim. Acta 2007, 71:5635-5650. 10.1016/j.gca.2006.12.022.
76. Roberts J.A. Inhibition and enhancement of microbial surface colonization: the role of silicate composition. Chem. Geol. 2004, 212:313-327. 10.1016/j.chemgeo.2004.08.021.
77. Roberts Rogers J., Bennett P., Choi W.J. Enhanced weathering of silicates by subsurface microorganisms: a strategy to release limiting inorganic nutrients?. Paper presented at Proceedings of the Tenth International Symposium On Water-Rock Interaction WRI-10 2001, 1461-1464.
78. Roberts J.A., Fowle D.A., Hughes B.T., Kulczycki E. Attachment behavior of Shewanella putrefaciens to magnetite under aerobic and anaerobic conditions. Geomicrobiol J. 2006, 23:631-640. 10.1080/01490450600964441.
79. Rogers J.R., Bennett P.C. Mineral stimulation of subsurface microorganisms: release of limiting nutrients from silicates. Chem. Geol. 2004, 203:91-108. 10.1016/j.chemgeo.2003.09.001.
80. Rogers J.R., Bennett P.C., Choi W.J. Feldspars as a source of nutrients for microorganisms. Am. Mineral. 1998, 83:1532-1540.
81. Rosling A. Responses of Ectomycorrhizal Fungi to Mineral Substrates 2003, PhD Thesis, Department of Forest Mycology and Pathology, Uppsala.
82. Rosling A., Lindahl B.D., Taylor A.F.S., Finlay R. Mycelial growth and substrate acidification of ectomycorrhizal fungi in response to different minerals. FEMS Microbiol. Ecol. 2004, 47:31-37. 10.1016/S0168-6496(03)00222-8.
83. Rufe E., Hochella M.F. Quantitative assessment of reactive surface area of phlogopite during acid dissolution. Science 1999, 285:874-876. 10.1126/science.285.5429.874.
84. Sazanova K.V., Shchiparev S.M., Vlasov D.Yu. Formation of organic acids by fungi isolated from the surface of stone monuments. Microbiology 2014, 83:525-533. 10.1134/S002626171405021X.
85. Sposito G. The Chemistry of Soils 1989, Oxford University Press, New York.
86. Taylor G.T., Troy P.J., Nullet M., Sharma S.K., Liebert B.E. Protein adsorption from seawater onto solid substrata: II. Behaviour of bound protein and its influence on interfacial properties. Mar. Chem. 1994, 47:21-39. 10.1016/0304-4203(94)90011-6.
87. Turpault M.-P., Trotignon L. The dissolution of biotite single crystals in dilute HNO3 at 24°C: evidence of an anisotropic corrosion process of micas in acidic solutions. Geochim. Cosmochim. Acta 1994, 58:2761-2775. 10.1016/0016-7037(94)90112-0.
88. Uroz S., Calvaruso C., Turpault M.-P., Pierrat J.-C., Mustin C., Frey-Klett P. Effect of the mycorrhizosphere on the genotypic and metabolic diversity of the bacterial communities involved in mineral-weathering in a forest soil. Appl. Environ. Microbiol. 2007, 73:3019-3027. 10.1128/AEM. 00121-07.
89. Uroz S., Calvaruso C., Turpault M.-P., Frey-Klett P. Mineral weathering by bacteria: ecology, actors and mechanisms. Trends Microbiol. 2009, 17:378-387. 10.1016/j.tim.2009.05.004.
90. Uroz S., Oger P., Lepleux C., Collignon C., Frey-Klett P., Turpault M.P. Bacterial weathering and its contribution to nutrient cycling in temperate forest ecosystems. Res. Microbiol. 2011, 162:820-831. 10.1016/j.resmic.2011.01.013.
91. Van Loosdrecht M.C.M., Lyklema J., Norde W., Zehnder A.J.B. Influence of interfaces on microbial activity. Microbiol. Rev. 1990, 54:75-87.
92. Welch S.A., Ullman W.J. The effect of microbial glucose metabolism on bytownite feldspar dissolution rates between 5 and 35C. Geochim. Cosmochim. Acta 1999, 63:3247-3259. 10.1016/S0016-7037(99)00248-3.
93. Welch S.A., Vandevivere P. Effect of microbial and other naturally occurring polymers on mineral dissolution. Geomicrobiol J. 1994, 12:227-238. 10.1080/01490459409377991.
94. Welch S.A., Barker W.W., Banfield J.F. Microbial extracellular polysaccharides and plagioclase dissolution. Geochim. Cosmochim. Acta 1999, 63:1405-1419. 10.1016/S0016-7037(99)00031-9.
95. White A.F., Blum A.E., Schulz M.S., Huntington T.G., Peters N.E., Stonestrom D.A. Chemical weathering of the Panola granite: solute and regolith elemental fluxes and the weathering rate of biotite. The Geochemical Society, Special Publication No. 7 2002, 37-59. R. Hellmann, S.A. Wood (Eds.).
96. Wu L., Jacobson A.D., Hausner M. Characterization of elemental release during microbe-granite interactions at T=28°C. Geochim. Cosmochim. Acta 2008, 72:1076-1095. 10.1016/j.gca.2007.11.025.
97. Zhen D., Taylor G.T., Gyananath G. Influence of laminar flow velocity and nutrient concentration on attachment of marine bacterioplankton. Biofouling 1994, 8:107-120. 10.1080/08927019409378266.