Bacterial weathering and its contribution to nutrient cycling in temperate forest ecosystems

Research in Microbiology

Volumn 162, Issue 9, 2011, Pages 820-831

  Uroz, Stéphane ^a,b   Oger, Phil ^c   Lepleux, Cendrella ^a,b   Collignon, Christelle ^a,b   Frey Klett, Pascale ^a   Turpault, Marie Pierre ^b  

^a UNIVERSITÉ DE LORRAINE   (France)

^b Centre INRA de Nancy   (France)

^c UNIVERSITÉ LYON 1   (France)

Author keywords

Bacterial communities; Forest; Mineral weathering; Nutrient cycling; Pyrosequencing; Soil

Indexed keywords

CARBON; MINERAL; NITROGEN;

ABIOTIC STRESS; ARTICLE; BIOTIC STRESS; BURKHOLDERIA; ECOLOGICAL NICHE; FOREST; FOREST MANAGEMENT; FOREST SOIL; MICROBIAL COMMUNITY; NUTRIENT CYCLING; PRIORITY JOURNAL; RHIZOSPHERE; SOIL CHEMISTRY; TEMPERATE DECIDUOUS FOREST; TREE; WEATHERING; BACTERIUM; CARBON CYCLE; CHEMISTRY; CLASSIFICATION; ECOSYSTEM; GENETICS; METABOLISM; MICROBIOLOGY; MYCORRHIZA; NITROGEN CYCLE; PHYLOGENY; PHYSIOLOGY; PLANT ROOT; SCANNING ELECTRON MICROSCOPY; SOIL; SYMBIOSIS; ULTRASTRUCTURE; WEATHER;

BACTERIA (MICROORGANISMS);

BACTERIA; CARBON CYCLE; ECOSYSTEM; MICROSCOPY, ELECTRON, SCANNING; MINERALS; MYCORRHIZAE; NITROGEN CYCLE; PHYLOGENY; PLANT ROOTS; SOIL; SOIL MICROBIOLOGY; SYMBIOSIS; TREES; WEATHER;

EID: 81355122645     PISSN: 09232508     EISSN: 17697123     Source Type: Journal    
DOI: 10.1016/j.resmic.2011.01.013     Document Type: Article

References (86)

1. Arocena J.M., Glowa K.R. Mineral-weathering in ectomycorrhizosphere of subalpine fir (Abies lasiocarpa (Hook.) Nutt.) as revealed by soil solution composition. For. Ecol. Manag. 2000, 133:61-70.
2. Augusto L., Turpault M.-P., Ranger J. Impact of forest tree species on feldspar weathering rates. Geoderma 2000, 96:215-237.
3. Ayres E., Steltzer H., Berg S., Wallenstein M.D., Simmons B.L., Wall D.H. Tree species traits influence soil physical, chemical, and biological properties in high elevation forests. PLoS One 2009, 4:e5964.
4. Balland C., Poswa A., Leyval C., Mustin C. Dissolution rates of phyllosilicates as a function of bacterial metabolic diversity. Geochim. Cosmochim. Acta 2010, 74:5478-5493.
5. 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.
6. Bini E. Archaeal transformation of metals in the environment. FEMS Microbiol. Ecol. 2010, 73:1-16.
7. Blum J.D., Klaue A., Nezat C.A., Driscoll C.T., Johnson C.E., Siccama T.G., Eagar C., Fahey T.J., Likens G.E. Mycorrhizal dissolution of apatite as an important calcium source in base-poor forest ecosystems. Nature 2002, 417:729-731.
8. Borin S., Ventura S., Tambone F., Mapelli F., Schubotz F., Brusetti L., Scaglia B., D'Acqui L.P., Solheim B., Turicchia S., Marasco R., Hinrichs K.U., Baldi F., Adani F., Daffonchio D. Rock weathering creates oases of life in a High Arctic desert. Environ. Microbiol. 2009, 12:293-303.
9. 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. Calvaruso C., Turpault M.-P., Leclerc E., Frey-Klett P. Impact of ectomycorrhizosphere on the functional diversity of soil bacterial and fungal communities from a forest stand in relation to nutrient mobilization processes. Microb. Ecol. 2007, 54:567-577.
11. Calvaruso C., Mareschal L., Turpault M.-P., Leclerc E. Rapid clay weathering in the rhizosphere of Norway spruce and oak in an acid forest ecosystem. Soil Sci. Soc. Am. J. 2009, 73:331-338.
12. Calvaruso C., Turpault M.-P., 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.
13. Carson J.K., Rooney D., Gleeson D.B., Clipson N. Altering the mineral composition of soil causes a shift in microbial community structure. FEMS Microbiol. Ecol. 2007, 61:414-423.
14. Certini G., Campbell C.D., Edwards A.C. Rock fragments in soil support a different microbial community from the fine earth. Soil Biol. Biochem. 2004, 36:1119-1128.
15. Cockell C.S., Olsson K., Herrera A., Meunier A. Alteration textures in terrestrial volcanic glass and the associated bacterial community. Geobiol 2009, 7:50-65.
16. Colin-Belgrand M., Dambrine E., Bienaimé S., Nys C., Turpault M.-P. Influence of tree roots on nitrogen mineralization. Scand. J. Forest Res. 2003, 18:260-268.
17. Courty P.-E., Buée M., Diedhiou A.G., Frey-Klett P., Le Tacon F., Rineau F., Turpault M.-P., Uroz S., Garbaye J. The role of ectomycorrhizal communities in forest ecosystem processes, new perspectives and emerging concepts. Soil Biol. Biochem. 2010, 42:679-698.
18. Dancis A., Klausner R.D., Hinnesbuch A.G., Barriocanal J.G. Genetic evidence that ferric reductase is required for iron uptake in Saccharomyces cerevisiae. Mol. Cell. Biol. 1990, 10:2294-2301.
19. de Boer W., Leveau J.H.J., Kowalchuk G.A., Klein Gunnewiek P.J.A., Abeln E.C.A., Figge M.J., et al. Collimonas fungivorans gen. nov., sp. nov., a chitinolytic soil bacterium with the ability to grow on living fungal hyphae. Int. J. Syst. Evol. Microbiol. 2004, 54:857-864.
20. 2-fixing bacterial diversity in soil under Acacia tortilis ssp. raddiana and Balanites aegyptiaca in the dryland part of Senegal. Environ. Microbiol. 2004, 6:400-415.
21. Drever J.I. Surface and Gound Water, Weathering, and Soils 2005, Elsevier, Amsterdam.
22. Frey P., Frey-Klett P., Garbaye J., Berge O., Heulin T. Metabolic and genotypic fingerprinting of fluorescent pseudomonads associated with the Douglas fir-Laccaria bicolor mycorrhizosphere. Appl. Environ. Microbiol. 1997, 63:1852-1860.
23. Frey-Klett P., Chavatte M., Clausse M.L., Courrier S., Le Roux C., Raaijmakers J., et al. Ectomycorrhizal symbiosis affects functional diversity of rhizosphere fluorescent pseudomonads. New Phytol. 2005, 165:317-328.
24. Gleeson D.B., Kennedy N.M., Clipson N., Melville K., Gadd G.M., McDermott F.P. Characterization of bacterial community structure on a weathered pegmatitic granite. Microb. Ecol. 2006, 51:526-534.
25. Goldstein A.H., Braverman K., Osorio N. Evidence for mutualism between a plant growing in a phosphate-limited desert environment and a mineral phosphate solubilizing (MPS) rhizobacterium. FEMS Microbiol. Ecol. 1999, 30:295-300.
26. Gorbushina A.A., Broughton W.J. Microbiology of the atmosphere-rock interface, how biological interactions and physical stresses modulate a sophisticated microbial ecosystem. Annu. Rev. Microbiol. 2009, 63:431-450.
27. Gray N.D., Hastings R.C., Sheppard S.K., Loughnane P., Lloyd D., McCarthy A.J., Head I.M. Effects of soil improvement treatments on bacterial community structure and soil processes in an upland grassland soil. FEMS Microbiol. Ecol. 2003, 46:11-22.
28. Grayston S.J., Vaughan D., Jones D. Rhizosphere carbon flow in trees, in comparison with annual plants, the importance of root exudation and its impact on microbial activity and nutrient availability. Appl. Soil Ecol. 1996, 5:29-56.
29. Gregory P.J., Hinsinger P. New approaches to studying chemical and physical changes in the rhizosphere, an overview. Plant Soil 1999, 211:1-9.
30. Höppener-Ogawa S., Leveau J.H.J., Smant W., van Veen J.A., de Boer W. Specific detection and real time PCR quantification of potentially mycophagous bacteria belonging to the genus Collimonas in different soil ecosystems. Appl. Environ. Microbiol. 2007, 73:4191-4197.
31. Haichar F.Z., Marol C., Berge O., Rangel-Castro J.I., Prosser J.I., Balesdent J., Heulin T., Achouak W. Plant host habitat and root exudates shape soil bacterial community structure. ISME J. 2008, 2:1221-1230.
32. 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.
33. Herrera A., Cockell C.S., Self S., Blaxter M., Reitner J., Arp G., Dröse W., Thorsteinsson T., Tindle A.G. Bacterial colonization and weathering of terrestrial obsidian in Iceland. Geomicrobiol. J. 2008, 25:25-37.
34. Herrera A., Cockell C.S., Self S., Blaxter M., Reitner J., Thorsteinsson T., Arp G., Drose W., Tindle A. A cryptoendolithic community in volcanic glass. Astrobiol 2009, 9:369-381.
35. Hinsinger P., Jaillard B. Root-induced release of interlayer potassium and vermicultization of phlogopite as related to potassium depletion in the rhizosphere of ryegrass. J. Soil Sci. 1993, 44:525-534.
36. Hutchens E. Microbial selectivity on mineral surfaces, possible implications for weathering processes. Fungal Biol. Rev. 2009, 10.1016/j.fbr.2009.10.002.
37. Hutchens E., Gleeson D., McDermott F., Miranda-CasolLuengo R., Clipson N. Meter-scale diversity of microbial communities on a weathered pegmatite granite outcrop in the wicklow mountains, Ireland, evidence for mineral induced selection?. Geomicrobiol. J. 2010, 27:1-14.
38. Jackson T.A., Voigt G.K. Biochemical weathering of calcium-bearing minerals by rhizosphere micro-organisms and its influence on calcium accumulation in trees. Plant Soil 1971, 35:655-658.
39. Jolivet C., Angers D.A., Chantigny M.H., Andreux F., Arrouays D. Carbohydrate dynamics in particle-size fractions of sandy spodosols following forest conversion to maize cropping. Soil Biol. Biochem. 2006, 38:2834-2842.
40. Kelly, L., Cockell, C.S., Piceno, Y.M., Anderson, G., Thorsteinsson, T., Marteinsson, V., 2010. Bacterial diversity of weathered terrestrial Icelandic volcanic glasses. Microbial. Ecol., in press.
41. Kim Y.H., Bae B., Choung Y.K. Optimization of biological phosphorus removal from contaminated sediments with phosphate-solubilizing microorganisms. J. Biosci. Bioeng. 2005, 99:23-29.
42. Kleinschmidt R., Hentschke I., Rothe M. Effect of season and soil treatments on carbohydrate concentrations in Norway spruce (Picea abies) mycorrhizae. Tree Physiol. 1998, 18:325-332.
43. Koele N., Turpault M.-P., Hildebrand E.E., Uroz S., Frey-Klett P. Interactions between mycorrhizal fungi and mycorrhizosphere bacteria during mineral-weathering, budget analysis and bacterial quantification. Soil Biol. Biochem. 2009, 41:1935-1942.
44. Landeweert R., Hoffland E., Finlay R.D., Kuyper T.W., van Breemen N. Linking plants to rock, ectomycorrhizal fungi mobilize nutrients from minerals. Trends Ecol. Evol. 2001, 16:248-253.
45. Lejon D.P.H., Chaussod R., Ranger J., Ranjard L. Microbial community structure and density under different tree species in an acid forest soil (Morvan, France). Microb. Ecol. 2005, 50:614-625.
46. Leveau J.H.J., Uroz S., de Boer W. The bacterial genus Collimonas, mycophagy, weathering and other adaptive solutions to life in oligotrophic soil environments. Environ. Microbiol. 2009, 10.1111/j.1462-2920.2009.02010.x.
47. Leyval C., Berthelin J. Interactions between Laccaria laccata, Agrobacterium radiobacter and beech roots, influence on P, K, Mg, and Fe mobilization from minerals and plant growth. Plant Soil 1989, 117:103-110.
48. Leyval C., Berthelin J. Weathering of a mica by roots and rhizospheric micro-organisms of pine. Soil Sci. Soc. Am. J. 1991, 55:1009-1016.
49. Liebeke M., Brözel V.S., Hecker M., Lalk M. Chemical characterization of soil extract as growth media for the ecophysiological study of bacteria. Appl. Microbiol. Biotechnol. 2009, 83:161-173.
50. 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.
51. Männistö M.K., Häggblom M.M. Characterization of psychrotolerant heterotrophic bacteria from Finnish Lapland. Syst. Appl. Microbiol. 2006, 29:229-243.
52. Martin F., Canet D., Marchal J.P. In vitro abundance 13C NMR studies of the carbohydrate storage in ectomycorrhizal fungi. Physiol. Vég. 1984, 22:733-743.
53. Medeiros P.M., Fernandes M.F., Dick R.P., Simoneit B.R.T. Seasonal variations in sugar contents and microbial community in a rye grass soil. Chemosphere 2006, 65:832-839.
54. Metcalfe A.C., Krsek M., Gooday G.W., Prosser J.I., Wellington E.M.H. Molecular analysis of a bacterial chitinolytic community in an upland pasture. Appl. Environ. Microbiol. 2002, 68:5042-5050.
55. Moore-Kucera J., Dick R.P. PLFA profiling of microbial community structure and seasonal shifts in soils of a Douglas-fir chronosequence. Microb. Ecol. 2008, 55:500-511.
56. Murataa T., Tanakaa H., Yasuea H., Hamadab R., Sakagamia K., Kurokawaa Y. Seasonal variations in soil microbial biomass content and soil neutral sugar composition in grassland in the Japanese temperate zone. Appl. Soil Ecol. 1999, 11:253-259.
57. Nambiar E.K.S. Sustained productivity of forest is a continuing challenge to soil science. Soil Sci. Soc. Am. J. 1997, 60:1629-1642.
58. 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.
59. Offre P., Pivato B., Siblot S., Gamalero E., Corberand T., Lemanceau P., Mougel C. Identification of bacterial groups preferentially associated with mycorrhizal roots of Medicago truncatula. Appl. Environ. Microbiol. 2007, 73:913-921.
60. Olsson P.A., Wallander H. Interactions between ectomycorrhizal fungi and the bacterial community in soils amended with various primary minerals. FEMS Microbiol. Ecol. 1998, 27:195-205.
61. Olsson-Francis K., de la Torre R., Cockell C.S. Isolation of novel extreme-tolerant cyanobacteria from a coastal rock-dwelling microbial community using exposure to low Earth orbit. Appl. Environ. Microbiol. 2010, 76:2115-2121.
62. +. Plant Soil 1996, 179:141-150.
63. Puente M.E., Li C.Y., Bashan Y. Microbial populations and activities in the rhizoplane of rock-weathering desert plants. II. Growth promotion of cactus seedlings. Plant Biol. 2004, 6:643-650.
64. Puente M.E., Bashan Y., Li C.Y., Lebsky V.K. Microbial populations and activities in the rhizoplane of rock-weathering desert plants. I. Root colonization and weathering of igneous rocks. Plant Biol. 2004, 6:629-642.
65. Puente M.E., Li C.Y., Bashan Y. Endophytic bacteria in cacti seeds can improve the development of cactus seedlings. Environ. Exp. Bot. 2009, 66:402-408.
66. Rangel-Castro J.I., Prosser J.I., Scrimgeour C.M., Smith P., Ostle N., Ineson P., Meharg A., Kilham K. Carbon flow in an upland grassland, effect of liming on the flux of recently photosynthesized carbon to rhizosphere soil. Global Change Biol. 2004, 10:2100-2108.
67. Ranger J., Turpault M.P. Input-output nutrient budgets as a diagnostic tool for sustainable forest management. For. Ecol. Manag. 1999, 122:139-154.
68. Séguin V., Courchesne F., Gagnon C., Martin R.R., Naftel S.J., Skinner W. Mineral-weathering in the rhizosphere of forested soils. Biogeochemistry of Trace Elements in the Rhizosphere 2005, 29-55. Chap. 2. P.M. Huang, G.R. Gobran (Eds.).
69. Santelli C.M., Edgcomb V.P., Bach W., Edwards K.J. The diversity and abundance of bacteria inhabiting seafloor lavas positively correlate with rock alteration. Environ. Microbiol. 2008, 11:86-98.
70. Sheppard K., Lloyd D. Effects of soil amendment on gas depth profiles in soil monoliths using direct mass spectrometric measurement. Bioresour. Technol. 2002, 84:39-47.
71. Thorseth I.H., Furnes H., Heldal M. The importance of microbiological activity in the alteration of natural basaltic glass. Geochim. Cosmochim. Acta 1992, 56:845-850.
72. 32P) and nutrient cycling. Appl. Environ. Microbiol. 1997, 63:4408-4412.
73. Turpault M.-P., Nys C., Calvaruso C. Rhizosphere impact on the dissolution of test minerals in a forest ecosystem. Geoderma 2009, 153:147-154.
74. Tyler G., Olsson T. Plant uptake of major and minor mineral elements as influenced by soil acidity and liming. Plant Soil 2001, 230:307-321.
75. 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 soil bacterial communities involved in mineral-weathering in a forest soil. Appl. Environ. Microbiol. 2007, 73:3019-3027.
76. Uroz S., Calvaruso C., Turpault M.-P., Frey-Klett P. The microbial weathering of soil minerals, ecology, actors and mechanisms. Trends Microbiol. 2009, 17:378-387.
77. Uroz S., Calvaruso C., Turpault M.-P., Sarniguet A., de Boer W., Leveau J.H.J., Frey-Klett P. Efficient mineral-weathering is a distinctive functional trait of the bacterial genus Collimonas. Soil Biol. Biochem. 2009, 41:2178-2186.
78. Uroz S., Buée M., Murat C., Frey-Klett P., Martin F. Pyrosequencing reveals a contrasted bacterial diversity between oak rhizosphere and surrounding soil. Environ. Microb. Rep. 2010, 2:281-288.
79. Uroz, S., Turpault, M.P., Delaruelle, C., Mareschal, L., Pierrat, J.-C., Frey-Klett, P. Minerals affect the specific diversity of forest soil bacterial communities. Geomicrobiol. J., in press.
80. Vasquez P., Holguin G., Puente M.E., Lopez-Cortez A., Bashan Y. Phosphate-solubilizing microorganisms associated with the rhizosphere of mangroves in a semiarid coastal lagoon. Biol. Fertil. Soils 2000, 30:460-468.
81. Vial L., Groleau M.-C., Dekimpe V., Déziel E. Burkholderia diversity and versatility, an inventory of the extracellular products. J. Microbiol. Biotechnol. 2007, 17:1407-1429.
82. Wallander H. Uptake of P from apatite by Pinus sylvestris seedlings colonised by different ectomycorrhizal fungi. Plant Soil 2000, 218:249-256.
83. White A.F., Brantley S.L. Chemical weathering rates of silicate minerals, an overview. Chemical Weathering Rates of Silicate Minerals 1995, 1-22. Mineralogical Society of America, Washington. A.F. White, S.L. Brantley (Eds.).
84. Wu L., Jacobson A.D., Chen H.S., Hausner M. Characterization of elemental release during microbe-basalt interactions at T = 28 °C. Geochim. Cosmochim. Acta 2007, 71:2224-2239.
85. 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.
86. Zeller B., Recous S., Kunze M., Moukoumi J., Colin-Belgrand M., Bienaimé S., Ranger J., Dambrine E. Influence of tree species on gross and net N transformation in forest soils. Ann. For. Sci. 2007, 64:151-158.