Abstract
Colonisation and weathering of freshly deglaciated granite are key processes in initial soil formation and development. We have obtained 438 isolates from granite sand covering glacial toe, 284 isolates at 22°C and 154 at 4°C incubation temperatures, respectively, to obtain cultures for the investigation of their weathering capabilities under laboratory conditions. The isolation of bacteria from granite sand was performed on rich-, intermediate- and low-nutrient-content solid media. Isolates were identified by 16S rRNA gene sequencing. According to the genera-associated weathering capabilities described in the literature and according to their abundance in our culture collection, we selected eight strains to analyse their effects on the weathering dynamics of granite sand during the batch culture experiment. Analysis of culturable bacteria showed higher species richness among isolates from 22°C than from 4°C incubations. In the R2A and 1/100 Ravan media, we observed the highest species richness of isolates obtained at 22°C and 4°C incubation temperatures, respectively. The obtained 16S rRNA sequences revealed the presence of alpha-, beta- and gamma-proteobacteria, Firmicutes, Actinobacteria and Bacteroidetes. The most numerous group of isolates was distantly related to Collimonas representatives, and according to the sequences of the 16S rRNA genes, they can form a new genus. Isolates from this group had the capability of causing increased dissolution rates for Fe, W, Ni and Rb. In general, at each sampling during the 30-day experiment, every strain showed a unique weathering profile resulting from differential rates of the dissolution and the precipitation of different minerals in the batch culture. Consequently, the presence of different strains, their growth stage and changes in proportions of strains in the bacterial community can affect further soil development and the successive colonisation by plants.








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References
Oerlemans J (2005) Extracting a climate signal from 169 glacier records. Science 308:675–677
Hodson A, Anesio A, Tranter M, Fountain A, Osborn M, Priscu J, Laybourn-Parry J, Sattler B (2008) Glacial ecosystems. Ecol Monogr 78:41–67
Segawa T, Miyamoto K, Ushida K, Agata K, Okada N, Kohshima S (2005) Seasonal change in bacterial flora and biomass in mountain snow from the Tateyama Mountains, Japan, analyzed by 16S rRNA gene sequencing and real-time PCR. Appl Environ Microbiol 71:123–130
Amato P, Parazols M, Sancelme M, Laj P, Mailhot G, Delort AM (2007) Microorganisms isolated from the water phase of tropospheric clouds at the Puy de Dome: major groups and growth abilities at low temperatures. FEMS Microbiol Ecol 59:242–254
Bauer H, Kasper-Giebl A, Löflund M, Giebl H, Hitzenberger R, Zibuschka F, Puxbaum H (2002) The contribution of bacteria and fungal spores to the organic carbon content of cloud water, precipitation and aerosols. Atmos Res 64:109–119
Bardgett RD, Richter A, Bol R, Garnett MH, Baumler R, Xu X, Lopez-Capel E, Manning DA, Hobbs PJ, Hartley IR, Wanek W (2007) Heterotrophic microbial communities use ancient carbon following glacial retreat. Biol Lett 3:487–490
Schmidt SK, Reed SC, Nemergut DR, Grandy AS, Cleveland CC, Weintraub MN, Hill AW, Costello EK, Meyer AF, Neff JC, Martin AM (2008) The earliest stages of ecosystem succession in high-elevation (5000 metres above sea level), recently deglaciated soils. Proc Biol Sci 275:2793–2802
Nemergut DR, Anderson SP, Cleveland CC, Martin AP, Miller AE, Seimon A, Schmidt SK (2007) Microbial community succession in an unvegetated, recently deglaciated soil. Microb Ecol 53:110–122
Sigler WV, Zeyer J (2002) Microbial diversity and activity along the forefields of two receding glaciers. Microb Ecol 43:397–407
Tscherko D, Rustemeier J, Richter A, Wanek W, Kandeler E (2003) Functional diversity of the soil microflora in primary succession across two glacier forelands in the Central Alps. Eur J Soil Sci 54:685–696
Schutte UME, Abdo Z, Bent SJ, Williams CJ, Schneider GM, Solheim B, Forney LJ (2009) Bacterial succession in a glacier foreland of the High Arctic. ISME J 3:1258–1268
Uroz S, Calvaruso C, Turpault MP, Pierrat JC, Mustin C, Frey-Klett P (2007) 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 73:3019–3027
Uroz S, Calvaruso C, Turpault MP, Frey-Klett P (2009) Mineral weathering by bacteria: ecology, actors and mechanisms. Trends Microbiol 17:378–387
Sharp M, Parkes J, Cragg B, Fairchild IJ, Lamb H, Tranter M (1999) Widespread bacterial populations at glacier beds and their relationship to rock weathering and carbon cycling. Geology 27:107–110
Tranter M, Sharp M, Lamb H, Brown G, Hubbard B, Willis I (2002) Geochemical weathering at the bed of Haut Glacier d’Arolla, Switzerland—a new model. Hydrol Process 16:959–993
Frey B, Rieder SR, Brunner I, Plotze M, Koetzsch S, Lapanje A, Brandl H, Furrer G (2010) Weathering-associated bacteria from the Damma glacier forefield: physiological capabilities and impact on granite dissolution. Appl Environ Microbiol 76:4788–4796
Borin S, Ventura S, Tambone F, Mapelli F, Schubotz F, Brusetti L, Scaglia B, D’Acqui LP, Solheim B, Turicchia S, Marasco R, Hinrichs KU, Baldi F, Adani F, Daffonchio D (2010) Rock weathering creates oases of life in a high Arctic desert. Environ Microbiol 12:293–303
Ferrari B, Binnerup S, Gillings M (2005) Microcolony cultivation on a soil substrate membrane system selects for previously uncultured soil bacteria. Appl Environ Microbiol 71:8714–8720
Janssen P, Yates P, Grinton B, Taylor P, Sait M (2002) Improved culturability of soil bacteria and isolation in pure culture of novel members of the divisions Acidobacteria, Actinobacteria, Proteobacteria, and Verrucomicrobia. Appl Environ Microbiol 68:2391–2396
Connon S, Giovannoni S (2002) High-throughput methods for culturing microorganisms in very-low-nutrient media yield diverse new marine isolates. Appl Environ Microbiol 68:3878–3885
Button D, Schut F, Quang P, Martin R, Robertson B (1993) Viability and isolation of marine bacteria by dilution culture: theory, procedures, and initial results. Appl Environ Microbiol 59:881–891
Goltekar R, Krishnan K, DeSouza M, Paropkari A, LokaBharathi P (2006) Effect of carbon source concentration and culture duration on retreivability of bacteria from certain estuarine, coastal and offshore areas around the peninsular India. Curr Sci 90:103–106p
Janssen P, Schuhmann A, Morschel E, Rainey F (1997) Novel anaerobic ultramicrobacteria belonging to the Verrucomicrobiales lineage of bacterial descent isolated by dilution culture from anoxic rice paddy soil. Appl Environ Microbiol 63:1382–1388
Goldberg J (2000) Pseudomonas: global bacteria. Trends Microbiol 8:55
Meyer AF, Lipson DA, Martin AP, Schadt CW, Schmidt SK (2004) Molecular and metabolic characterization of cold-tolerant alpine soil Pseudomonas sensu stricto. Appl Environ Microbiol 70:483–489
Tindall B (2004) Prokaryotic diversity in the Antarctic: the tip of the iceberg. Microb Ecol 47:271–283
Edwards I, Bürgmann H, Miniaci C, Zeyer J (2006) Variation in microbial community composition and culturability in the rhizosphere of Leucanthemopsis alpina (L.) Heywood and adjacent bare soil along an alpine chronosequence. Microb Ecol 52:679–692
Moreno F, Vilela S, Antunes Â, Alves C (2006) Capillary-rising salt pollution and granitic stone erosive decay in the parish church of Torre de Moncorvo (NE Portugal)—implications for conservation strategy. J Cult Herit 7:56–66
Franzen C, Mirwald P (2004) Moisture content of natural stone: static and dynamic equilibrium with atmospheric humidity. Environ Geol 46:391–401
Gorbushina AA (2007) Life on the rocks. Environ Microbiol 9:1613–1631
Deo N, Vasan S, Modak JM, Natarajan K (1999) Selective biodissolution of calcium and iron from bauxite in the presence of Bacillus polymyxa. Process Metall 9:463–472
Vasan S, Modak JM, Natarajan K (2001) Some recent advances in the bioprocessing of bauxite. Int J Miner Process 62:173–186
Lazzaro A, Abegg C, Zeyer J (2009) Bacterial community structure of glacier forefields on siliceous and calcareous bedrock. Eur J Soil Sci 60:860–870
Noll M, Wellinger M (2008) Changes of the soil ecosystem along a receding glacier: testing the correlation between environmental factors and bacterial community structure. Soil Biol Biochem 40:2611–2619
Taylor RH, Geldreich EE (1976) A new membrane filter procedure for bacterial counts in potable water and swimming pool samples. J Am Water Works Assoc 38:191
Greenberg AE (1981) Standard methods for the examination of water and wastewater. American Public Health Association, Washington
Reasoner D, Geldreich E (1985) A new medium for the enumeration and subculture of bacteria from potable water. Appl Environ Microbiol 49:1
Logan N, Moss M (1992) Identification of Chromobacterium, Janthinobacterium and Iodobacter species. Soc Appl Bacteriol Techn Ser 29:183–192
Watve M, Shejval V, Sonawane C, Rahalkar M, Matapurkar A, Shouche Y, Patole M, Phadnis N, Champhenkar A, Damle K (2000) The ‘K’ selected oligophilic bacteria: a key to uncultured diversity? Curr Sci 78:1535–1542
Giraffa G, Rossetti L, Neviani E (2000) An evaluation of chelex-based DNA purification protocols for the typing of lactic acid bacteria. J Microbiol Methods 42:175–184
Lapanje A, Zrimec A, Drobne D, Rupnik M (2010) Long-term Hg pollution-induced structural shifts of bacterial community in the terrestrial isopod (Porcellio scaber) gut. Environ Pollut 158:3186–3193
Bianciotto V, Bandi C, Minerdi D, Sironi M, Tichy HV, Bonfante P (1996) An obligately endosymbiotic mycorrhizal fungus itself harbors obligately intracellular bacteria. Appl Environ Microbiol 62:3005–3010
Heuer H, Krsek M, Baker P, Smalla K, Wellington EM (1997) Analysis of actinomycete communities by specific amplification of genes encoding 16S rRNA and gel-electrophoretic separation in denaturing gradients. Appl Environ Microbiol 63:3233–3241
Teske A, Wawer C, Muyzer G, Ramsing NB (1996) Distribution of sulfate-reducing bacteria in a stratified fjord (Mariager Fjord, Denmark) as evaluated by most-probable-number counts and denaturing gradient gel electrophoresis of PCR-amplified ribosomal DNA fragments. Appl Environ Microbiol 62:1405–1415
Cheng S, Foght J (2007) Cultivation-independent and -dependent characterization of bacteria resident beneath John Evans Glacier. FEMS Microbiol Ecol 59:318–330
Liermann LJ, Kalinowski BE, Brantley SL, Ferry JG (2000) Role of bacterial siderophores in dissolution of hornblende. Geochim Cosmochim Acta 64:587–602
Viollier E, Inglett P, Hunter K, Roychoudhury A, Van Cappellen P (2000) The ferrozine method revisited: Fe(II)/Fe(III) determination in natural waters. Appl Geochem 15:785–790
Larkin M, Blackshields G, Brown N, Chenna R, McGettigan P, McWilliam H, Valentin F, Wallace I, Wilm A, Lopez R (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23:2947
Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596
Holland S (1988) A rarefactwin program, version 1.2. http://www.uga.edu/strata/Software.html
Raffl C, Mallaun M, Mayer R, Erschbamer B (2006) Vegetation succession pattern and diversity changes in a glacier valley, Central Alps, Austria. Arct Antarct Alp Res 38:421–428
Kalinowski BE, Liermann LJ, Givens S, Brantley SL (2000) Rates of bacteria-promoted solubilization of Fe from minerals: a review of problems and approaches. Chem Geol 169:357–370
Banfield JF, Barker WW, Welch SA, Taunton A (1999) Biological impact on mineral dissolution: application of the lichen model to understanding mineral weathering in the rhizosphere. Proc Natl Acad Sci U S A 96:3404
Barshad I, Kishk FM (1968) Oxidation of ferrous iron in vermiculite and biotite alters fixation and replaceability of potassium. Science 162:1401
Murakami T, Utsunomiya S, Yokoyama T, Kasama T (2003) Biotite dissolution processes and mechanisms in the laboratory and in nature: early stage weathering environment and vermiculitization. Am Mineral 88:377
Faramarzi MA, Brandl H (2006) Formation of water soluble metal cyanide complexes from solid minerals by Pseudomonas plecoglossicida. FEMS Microbiol Lett 259:47–52
Kletzin A, Adams MWW (1996) Tungsten in biological systems. FEMS Microbiol Rev 18:5–63
Wichard T, Bellenger JP, Loison A, Kraepiel AML (2008) Catechol siderophores control tungsten uptake and toxicity in the nitrogen-fixing bacterium Azotobacter vinelandii. Environ Sci Technol 42:2408–2413
Wu L, Jacobson AD, Hausner M (2008) Characterization of elemental release during microbe–granite interactions at T = 28°C. Geochim Cosmochim Acta 72:1076–1095
Hausrath EM, Neaman A, Brantley SL (2009) Elemental release rates from dissolving basalt and granite with and without organic ligands. Am J Sci 309:633
Taunton AE, Welch SA, Banfield JF (2000) Microbial controls on phosphate and lanthanide distributions during granite weathering and soil formation. Chem Geol 169:371–382
Kiczka M, Wiederhold JG, Frommer J, Kraemer SM, Bourdon B, Kretzschmar R (2010) Iron isotope fractionation during proton- and ligand-promoted dissolution of primary phyllosilicates. Geochim Cosmochim Acta 74:3112–3128
Luu YS, Ramsay JA (2003) Review: microbial mechanisms of accessing insoluble Fe(III) as an energy source. World J Microbiol Biotechnol 19:215–225
Liu W, Fisher SM, Wells JS Jr, Ricca CS, Principe PA, Trejo WH, Bonner DP, Gougoutos JZ, Toeplitz BK, Sykes RB (1981) Siderochelin, a new ferrous-ion chelating agent produced by Nocardia. J Antibiot 34:791
Short NM (1961) Geochemical variations in four residual soils. J Geol 69:534–571
Kabata-Pendias A, Pendias H (2001) Trace elements in soils and plants. CRC, Boca Raton
Kabata-Pendias A (2001) Trace elements in soils and plants. CRC Press, Inc., Boca Raton, Florida, 413 pp
Ashworth DJ, Alloway BJ (2008) Influence of dissolved organic matter on the solubility of heavy metals in sewage-sludge-amended soils. Commun Soil Sci Plan 39:538
Smith IC, Carson BL (1978) Trace metals in the environment. Volume 3 – Zirconium. Ann Arbor Science Publishers Inc., Ann Arbor, Michigan, 405 pp
Brookins DG (1988) Eh-pH diagrams for geochemistry. Springer-Verlag, Berlin-Heidelberg, 176 pp
Männisto MK, Häggblom MM (2006) Characterization of psychrotolerant heterotrophic bacteria from Finnish Lapland. Syst Appl Microbiol 29:229–243
Schmidt SK, Nemergut DR, Miller AE, Freeman KR, King AJ, Seimon A (2009) Microbial activity and diversity during extreme freeze–thaw cycles in periglacial soils, 5400 m elevation, Cordillera Vilcanota, Peru. Extremophiles 13:807–816
Liu Y, Yao T, Jiao N, Kang S, Huang S, Li Q, Wang K, Liu X (2009) Culturable bacteria in glacial meltwater at 6,350 m on the East Rongbuk Glacier, Mount Everest. Extremophiles 13:89–99
Foght J, Aislabie J, Turner S, Brown C, Ryburn J, Saul D, Lawson W (2004) Culturable bacteria in subglacial sediments and ice from two southern hemisphere glaciers. Microb Ecol 47:329–340
Lipson DA, Schmidt SK (2004) Seasonal changes in an alpine soil bacterial community in the Colorado Rocky Mountains. Appl Environ Microbiol 70:2867–2879
Zhang G, Niu F, Ma X, Liu W, Dong M, Feng H, An L, Cheng G (2007) Phylogenetic diversity of bacteria isolates from the Qinghai–Tibet Plateau permafrost region. Can J Microbiol 53:1000–1010
Brinkmeyer R, Knittel K, Jurgens J, Weyland H, Amann R, Helmke E (2003) Diversity and structure of bacterial communities in Arctic versus Antarctic pack ice. Appl Environ Microbiol 69:6610–6619
Skidmore M, Anderson SP, Sharp M, Foght J, Lanoil BD (2005) Comparison of microbial community compositions of two subglacial environments reveals a possible role for microbes in chemical weathering processes. Appl Environ Microbiol 71:6986–6997
Christner BC, Mosley-Thompson E, Thompson LG, Reeve JN (2003) Bacterial recovery from ancient glacial ice. Environ Microbiol 5:433–436
Miteva VI, Sheridan PP, Brenchley JE (2004) Phylogenetic and physiological diversity of microorganisms isolated from a deep Greenland glacier ice core. Appl Environ Microbiol 70:202–213
Miskin I, Rhodes G, Lawlor K, Saunders JR, Pickup RW (1998) Bacteria in post-glacial freshwater sediments. Microbiology 144(Pt 9):2427–2439
Mikucki JA, Priscu JC (2007) Bacterial diversity associated with Blood Falls, a subglacial outflow from the Taylor Glacier, Antarctica. Appl Environ Microbiol 73:4029–4039
Christner BC, Kvitko BH 2nd, Reeve JN (2003) Molecular identification of bacteria and Eukarya inhabiting an Antarctic cryoconite hole. Extremophiles 7:177–183
Zhang G, Ma X, Niu F, Dong M, Feng H, An L, Cheng G (2007) Diversity and distribution of alkaliphilic psychrotolerant bacteria in the Qinghai–Tibet Plateau permafrost region. Extremophiles 11:415–424
Black E, Wei J, Atluri S, Cortezzo D, Koziol-Dube K, Hoover D, Setlow P (2007) Analysis of factors influencing the rate of germination of spores of Bacillus subtilis by very high pressure. J Appl Microbiol 102:65–76
Gorbushina A, Kort R, Schulte A, Lazarus D, Schnetger B, Brumsack H, Broughton W, Favet J (2007) Life in Darwin’s dust: intercontinental transport and survival of microbes in the nineteenth century. Environ Microbiol 9:2911–2922
Sattler B, Puxbaum H, Psenner R (2001) Bacterial growth in supercooled cloud droplets. Geophys Res Lett 28:239–242
Steven B, Léveillé R, Pollard W, Whyte L (2006) Microbial ecology and biodiversity in permafrost. Extremophiles 10:259–267
Panikov N, Sizova M (2006) Growth kinetics of microorganisms isolated from Alaskan soil and permafrost in solid media frozen down to −35°C. FEMS Microbiol Ecol 59:500–512
Yuhana M (2005) Microbial diversity and community changes in high mountain habitats (2009) PhD thesis, ETH Zurich
Vandamme P, Pot B, Gillis M, De Vos P, Kersters K, Swings J (1996) Polyphasic taxonomy, a consensus approach to bacterial systematics. Microbiol Mol Biol Rev 60:407
Acknowledgements
Financial support for this study was provided by the BigLink project of the Competence Center Environment and Sustainability (CCES) of the ETH Domain. This study was also supported by the Genetic Diversity Centre of ETH Zurich (GDC). Helmut Brandl (University of Zurich) and Daniela Steiner (WSL) are acknowledged for the valuable scientific and technical support.
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Supplement Figure 1
Phylogenetic position of the 16S rRNA genes of isolates. Here are selected isolates that have lower than 98% similarities among the RDPII database isolates and type strains of Burkholderiales. Collimonas relatives are here excluded. Numbers on the branches represent bootstrap values. Isolates are presented in bold numbers. Black-filled circles represent 4°C isolates. Tree is constructed with a neighbour joining method based on Kimura two-parameter distance values (DOC 507 kb)
Supplement Figure 2
Isolate preferences in dissolving different elements from the granite sand. Figures show principal component analysis (PCA) of the concentrations of elements in each batch reactor. Vectors specify multidimensional space determined by the variations in elements concentrations in batch reactors. Yellow numbers in blue circles show the mean scores of three batches per isolate (DOC 10472 kb)
Supplement Table 1a
Characteristics of isolates obtained at 22°C (DOC 772 kb)
Supplement Table 2
Dissolution rates of elements from the granite sand during the 30-day experiment. Red-coloured elements with arrows pointing up show the increase and blue-coloured elements with down-pointing arrows the decrease of dissolution rate according to the control. *90% confidence interval, **95% confidence interval, ***99% confidence interval in pairwise Student’s t tests (DOC 57 kb)
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Lapanje, A., Wimmersberger, C., Furrer, G. et al. Pattern of Elemental Release During the Granite Dissolution Can Be Changed by Aerobic Heterotrophic Bacterial Strains Isolated from Damma Glacier (Central Alps) Deglaciated Granite Sand. Microb Ecol 63, 865–882 (2012). https://doi.org/10.1007/s00248-011-9976-7
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DOI: https://doi.org/10.1007/s00248-011-9976-7


