Weathering-Associated Bacteria from the Damma Glacier Forefield: Physiological Capabilities and Impact on Granite Dissolution

ABSTRACT Several bacterial strains isolated from granitic rock material in front of the Damma glacier (Central Swiss Alps) were shown (i) to grow in the presence of granite powder and a glucose-NH4Cl minimal medium without additional macro- or micronutrients and (ii) to produce weathering-associated agents. In particular, four bacterial isolates (one isolate each of Arthrobacter sp., Janthinobacterium sp., Leifsonia sp., and Polaromonas sp.) were weathering associated. In comparison to what was observed in abiotic experiments, the presence of these strains caused a significant increase of granite dissolution (as measured by the release of Fe, Ca, K, Mg, and Mn). These most promising weathering-associated bacterial species exhibited four main features rendering them more efficient in mineral dissolution than the other investigated isolates: (i) a major part of their bacterial cells was attached to the granite surfaces and not suspended in solution, (ii) they secreted the largest amounts of oxalic acid, (iii) they lowered the pH of the solution, and (iv) they formed significant amounts of HCN. As far as we know, this is the first report showing that the combined action of oxalic acid and HCN appears to be associated with enhanced elemental release from granite, in particular of Fe. This suggests that extensive microbial colonization of the granite surfaces could play a crucial role in the initial soil formation in previously glaciated mountain areas.

[1]  W. Haeberli,et al.  Initial stages of weathering and soil formation in the Morteratsch proglacial area (Upper Engadine, Switzerland) , 2010 .

[2]  W. Boer,et al.  Efficient mineral weathering is a distinctive functional trait of the bacterial genus Collimonas , 2009 .

[3]  G. Furrer,et al.  Effect of iron and phosphate on bacterial cyanide formation determined by methemoglobin in two-dimensional gradient microcultivations. , 2009, Journal of microbiological methods.

[4]  W. Broughton,et al.  Microbiology of the atmosphere-rock interface: how biological interactions and physical stresses modulate a sophisticated microbial ecosystem. , 2009, Annual review of microbiology.

[5]  Y. Bashan,et al.  Rock-degrading endophytic bacteria in cacti , 2009 .

[6]  P. Frey-Klett,et al.  Mineral weathering by bacteria: ecology, actors and mechanisms. , 2009, Trends in microbiology.

[7]  S. Bernasconi,et al.  Weathering, soil formation and initial ecosystem evolution on a glacier forefield: a case study from the Damma Glacier, Switzerland , 2008, Mineralogical Magazine.

[8]  M. Hoelzle,et al.  Integrated monitoring of mountain glaciers as key indicators of global climate change: the European Alps , 2007, Annals of Glaciology.

[9]  A. Jacobson,et al.  Characterization of elemental release during microbe–granite interactions at T = 28 °C , 2007 .

[10]  J. Pierrat,et al.  Effect of the Mycorrhizosphere on the Genotypic and Metabolic Diversity of the Bacterial Communities Involved in Mineral Weathering in a Forest Soil , 2007, Applied and Environmental Microbiology.

[11]  C. Rensing.  Microorganisms and Earth Systems—Advances in Geomicrobiology , 2007 .

[12]  Yukinori Matsukura,et al.  Effect of Bacillus subtilis on granite weathering: A laboratory experiment , 2006 .

[13]  H. Bürgmann,et al.  Variation in Microbial Community Composition and Culturability in the Rhizosphere of Leucanthemopsis alpina (L.) Heywood and Adjacent Bare Soil Along an Alpine Chronosequence , 2006, Microbial Ecology.

[14]  M. Faramarzi,et al.  Formation of water-soluble metal cyanide complexes from solid minerals by Pseudomonas plecoglossicida. , 2006, FEMS microbiology letters.

[15]  S. Brantley,et al.  The coupling of biological iron cycling and mineral weathering during saprolite formation, Luquillo Mountains, Puerto Rico , 2005 .

[16]  T. Egli,et al.  New method for assimilable organic carbon determination using flow-cytometric enumeration and a natural microbial consortium as inoculum. , 2005, Environmental science & technology.

[17]  J. Oerlemans.  Extracting a Climate Signal from 169 Glacier Records , 2005, Science.

[18]  Y. Bashan,et al.  Microbial populations and activities in the rhizoplane of rock-weathering desert plants. I. Root colonization and weathering of igneous rocks. , 2004, Plant biology.

[19]  A. Anbar,et al.  Fe isotopic fractionation during mineral dissolution with and without bacteria , 2004 .

[20]  J. Chorover,et al.  Effects of organic ligands on granite dissolution in batch experiments at pH 6 , 2004, American Journal of Science.

[21]  M. Caccianiga,et al.  Pioneer herbaceous vegetation on glacier forelands in the Italian Alps , 2004 .

[22]  W. Wanek,et al.  Functional diversity of the soil microflora in primary succession across two glacier forelands in the Central Alps , 2003 .

[23]  J. Banfield,et al.  Effect of Microorganisms and Microbial Metabolites on Apatite Dissolution , 2002 .

[24]  P. Janssen,et al.  Improved Culturability of Soil Bacteria and Isolation in Pure Culture of Novel Members of the Divisions Acidobacteria, Actinobacteria, Proteobacteria, and Verrucomicrobia , 2002, Applied and Environmental Microbiology.

[25]  J. Zeyer,et al.  Microbial Diversity and Activity along the Forefields of Two Receding Glaciers , 2002, Microbial Ecology.

[26]  T. R. Clark,et al.  Biogenic production of cyanide and its application to gold recovery , 2001, Journal of Industrial Microbiology and Biotechnology.

[27]  M. Watve,et al.  The 'K' selected oligophilic bacteria: a key to uncultured diversity? , 2000 .

[28]  J. Fein,et al.  Experimental study of the effects of Bacillus subtilis on gibbsite dissolution rates under near-neutral pH and nutrient-poor conditions , 2000 .

[29]  S. P. Anderson,et al.  Chemical weathering in the foreland of a retreating glacier , 2000 .

[30]  C. Pantano,et al.  X-ray photoelectron evidence for bacteria-enhanced dissolution of hornblende , 2000 .

[31]  Dieter Haas,et al.  Mechanism, regulation, and ecological role of bacterial cyanide biosynthesis , 2000, Archives of Microbiology.

[32]  J. Ferry,et al.  Role of bacterial siderophores in dissolution of hornblende , 2000 .

[33]  S. Welch,et al.  The effect of microbial glucose metabolism on bytownite feldspar dissolution rates between 5 and 35 C , 1999 .

[34]  J. Banfield,et al.  Microbial extracellular polysaccharides and plagioclase dissolution , 1999 .

[35]  J. Banfield,et al.  Biological impact on mineral dissolution: application of the lichen model to understanding mineral weathering in the rhizosphere. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[36]  J. Banfield,et al.  Experimental observations of the effects of bacteria on aluminosilicate weathering , 1998 .

[37]  David L. Kirchman,et al.  Laboratory evidence for microbially mediated silicate mineral dissolution in nature , 1996 .

[38]  C. Bandi,et al.  An obligately endosymbiotic mycorrhizal fungus itself harbors obligately intracellular bacteria , 1996, Applied and environmental microbiology.

[39]  J. Neilands,et al.  Siderophores: Structure and Function of Microbial Iron Transport Compounds (*) , 1995, The Journal of Biological Chemistry.

[40]  L. Bakken,et al.  Evaluation of methods for extraction of bacteria from soil , 1995 .

[41]  G. Furrer,et al.  The coordination chemistry of weathering: I. Dissolution kinetics of δ-Al2O3 and BeO , 1986 .

[42]  Harold C. Bold,et al.  The Morphology of Chlamydomonas chlamydogama, Sp. Nov. , 1949 .

[43]  M.,et al.  Microbial Populations and Activities in the Rhizoplane of Rock-Weathering Desert Plants. I. Root Colonization and Weathering of Igneous Rocks , 2006 .

[44]  L. Warren.  Micro-organisms and earth systems – advances in geomicrobiology: Biofilms and metal geochemistry: the relevance of micro-organism-induced geochemical transformations , 2005 .

[45]  P. Bennett,et al.  Silicates, Silicate Weathering, and Microbial Ecology , 2001 .

[46]  S. Brantley,et al.  Uptake of Trace Metals and Rare Earth Elements from Hornblende by a Soil Bacterium , 2001 .

[47]  J. Neilands,et al.  Universal chemical assay for the detection and determination of siderophores. , 1987, Analytical biochemistry.

[48]  A. Bunch,et al.  Microbial cyanide metabolism. , 1986, Advances in microbial physiology.

[49]  A. Vuorinen,et al.  Bacterial weathering of rapakivi granite , 1981 .