Download PDF
Plant Biol (Stuttg) 2004; 6(5): 629-642
DOI: 10.1055/s-2004-821100
Original Paper

Georg Thieme Verlag Stuttgart KG · New York

Microbial Populations and Activities in the Rhizoplane of Rock-Weathering Desert Plants. I. Root Colonization and Weathering of Igneous Rocks

M. E. Puente1 , Y. Bashan1 , C. Y. Li2 , V. K. Lebsky1
  • 1Environmental Microbiology Group, Center for Biological Research of the Northwest (CIB), P.O. Box 128, La Paz, B.C.S. 23000, Mexico,
  • 2USDA Forest Service, Pacific Northwest Research Station, Forestry Sciences Laboratory, 3200 SW Jefferson Way, Corvallis, Oregon 97331, USA
Further Information

Publication History

Publication Date:
12 August 2004 (online)

   Permissions and Reprints

Abstract

Dense layers of bacteria and fungi in the rhizoplane of three species of cactus (Pachycereus pringlei, Stenocereus thurberi, Opuntia cholla) and a wild fig tree (Ficus palmeri) growing in rocks devoid of soil were revealed by bright-field and fluorescence microscopy and field emission scanning electron microscopy. These desert plants are responsible for rock weathering in an ancient lava flow at La Purisima-San Isidro and in sedimentary rock in the Sierra de La Paz, both in Baja California Sur, Mexico. The dominant bacterial groups colonizing the rhizoplane were fluorescent pseudomonads and bacilli. Seven of these bacterial species were identified by the 16S rRNA molecular method. Unidentified fungal and actimomycete species were also present. Some of the root-colonizing microorganisms fixed in vitro N2, produced volatile and non-volatile organic acids that subsequently reduced the pH of the rock medium in which the bacteria grew, and significantly dissolved insoluble phosphates, extrusive igneous rock, marble, and limestone. The bacteria were able to release significant amounts of useful minerals, such as P, K, Mg, Mn, Fe, Cu, and Zn from the rocks and were thermo-tolerant, halo-tolerant, and drought-tolerant. The microbial community survived in the rhizoplane of cacti during the annual 10-month dry season. This study indicates that rhizoplane bacteria on cacti roots in rock may be involved in chemical weathering in hot, subtropical deserts.

Key words

Bacillus - cactus - cardon - cholla - desert - Ficus - fig tree - fluorescent pseudomonads - lava degradation - nitrogen fixation - Opuntia - Pachycereus - phosphate solubilization - rock weathering - soil formation - Stenocereus.

References

  • 1 Adams J. B., Palmer F., Staley J. T.. Rock weathering in deserts: mobilization and concentration of ferric iron by microorganisms.  Geomicrobiology Journal. (1992);  10 99-114
    PubMedSearch in Google Scholar
  • 2 Ascaso C., Sancho L. G., Rodriguez Pascual C.. The weathering action of saxicolous lichens in maritime Antarctica.  Polar Biology. (1990);  11 33-40
    PubMedSearch in Google Scholar
  • 3 Barker W. W., Banfield J. F.. Zones of chemical and physical interaction at interfaces between microbial communities and minerals: a model.  Geomicrobiology Journal. (1998);  15 223-244
    PubMedSearch in Google Scholar
  • 4 Bashan Y., Davis E. A., Carrillo-Garcia A., Linderman R. G.. Assessment of VA mycorrhizal inoculum potential in relation to the establishment of cactus seedlings under mesquite nurse-trees in the Sonoran desert.  Applied Soil Ecology. (2000);  14 165-176
    CrossrefPubMedSearch in Google Scholar
  • 5 Bashan Y., Levanony H., Whitmoyer R. E.. Root surface colonization of non-cereal crop plants by pleomorphic Azospirillum brasilense. .  Journal of General Microbiology. (1991);  137 187-196
    PubMedSearch in Google Scholar
  • 6 Bashan Y., Li C. Y., Lebsky V. K., Moreno M., de-Bashan L. E.. Primary colonization of volcanic rocks by plants in arid Baja California, Mexico.  Plant Biology. (2002);  4 392-402
    Thieme ConnectPubMedSearch in Google Scholar
  • 7 Bashan Y., Rojas A., Puente M. E.. Improved establishment and development of three cacti species inoculated with Azospirillum brasilense transplanted into disturbed urban desert soil.  Canadian Journal of Microbiology. (1999);  45 441-451
    CrossrefPubMedSearch in Google Scholar
  • 8 Berthelin J., Leyval C., Laheurte F., Giudici  de. P.. Involvement of roots and rhizosphere microflora in the chemical weathering of soil minerals. Atkinson, D., ed. Plant Root Growth: An Ecological Perspective. Oxford, UK; Blackwell Scientific Publications (1991): 187-200
    Search in Google Scholar
  • 9 Carrillo A. E., Li C. Y., Bashan Y.. Increased acidification in the rhizosphere of cactus seedlings induced by Azospirillum brasilense. .  Naturwissenschaften. (2002);  89 428-432
    CrossrefPubMedSearch in Google Scholar
  • 10 Carrillo-Garcia A., Bashan Y., Bethlenfalvay G. J.. Resource-island soils and the survival of the giant cactus cardon of Baja California Sur.  Plant and Soil. (2000 a);  218 207-214
    CrossrefPubMedSearch in Google Scholar
  • 11 Carrillo-Garcia A., Bashan Y., Diaz-Rivera E., Bethlenfalvay G. J.. Effects of resource-island soils, competition, and inoculation with Azospirillum on survival and growth of Pachycereus pringlei, the giant cactus of the Sonoran desert.  Restoration Ecology. (2000 b);  8 65-73
    CrossrefPubMedSearch in Google Scholar
  • 12 Carrillo-Garcia A., Leon de la Luz J. L., Bashan Y., Bethlenfalvay G. J.. Nurse plants, mycorrhizae, and plant establishment in a disturbed area of the Sonoran desert.  Restoration Ecology. (1999);  7 321-335
    CrossrefPubMedSearch in Google Scholar
  • 13 Chabot R., Antoun H., Cescas M. P.. Growth promotion of maize and lettuce by phosphate-solubilizing Rhizobium legominosarum biovar. phaseoli. .  Plant and Soil. (1996);  184 311-321
    PubMedSearch in Google Scholar
  • 14 Chang T. T., Li C. Y.. Weathering of limestone, marble, and calcium phosphate by ectomycorrhizal fungi and associated microorganisms.  Taiwan Journal of Forest Science. (1998);  13 85-90
    PubMedSearch in Google Scholar
  • 15 Dahanayake K., Subasinghe S. M. N. D.. Formation of phosphatic coated grains and peloids by grain diminution of Precambrian apatite crystals.  Journal of Geological Society of India. (1990);  35 189-202
    PubMedSearch in Google Scholar
  • 16 Danin A.. Pitting of calcareus rocks by organisms under terrestrial conditions.  Israel Journal of Earth Science. (1993);  41 201-207
    PubMedSearch in Google Scholar
  • 17 Danin A., Caneva G.. Deterioration of limestone walls in Jerusalem and marble monuments in Rome caused by cyanobacteria and cyanophilous lichens.  International Biodeterioration. (1990);  26 397-417
    CrossrefPubMedSearch in Google Scholar
  • 18 De la Torre M. A., Gomez-Alarcon G., Palacios J. M.. “In vitro” biofilm formation by Penicillium frequentans strain on sandstone, granite, and limestone.  Applied Microbiology Biotechnology. (1993);  40 408-415
    PubMedSearch in Google Scholar
  • 19 Ferris F. G., Lowson E. A.. Ultrastructure and geochemistry of endolithic microorganisms in limestone of the Niagara Escarpment.  Canadian Journal of Microbiology. (1997);  43 211-219
    PubMedSearch in Google Scholar
  • 20 Flores M., Lorenzo J., Gomez-Alarcon G.. Algae and bacteria on historic monuments at Alcala de Henares, Spain.  International Biodeterioration and Biodegradation. (1997);  40 241-246
    CrossrefPubMedSearch in Google Scholar
  • 21 Franco A. C., Nobel P. S.. Effect of nurse plants on the microhabitat and growth of cacti.  Journal of Ecology. (1989);  77 870-886
    PubMedSearch in Google Scholar
  • 22 Friedmann E. I.. Endolithic microorganisms in the Antarctic cold desert.  Science. (1982);  215 1045-1053
    PubMedSearch in Google Scholar
  • 23 Friedmann E. I., Kibler A. P.. Nitrogen economy of endolithic microbial communities in hot and cold deserts.  Microbial Ecology. (1980);  6 95-108
    PubMedSearch in Google Scholar
  • 24 Goudie A. S., Parker A. G.. Experimental simulation of rapid rock block disintegration by sodium chloride in a foggy coastal desert.  Journal of Arid Environment. (1999);  40 347-355
    PubMedSearch in Google Scholar
  • 25 Gyaneshwar P., Kumar G. N., Parekh L. J.. Effect of buffering on the phosphate-solubilizing ability of microorganism.  World Journal of Microbiology Biotechnology. (1998);  14 669-673
    PubMedSearch in Google Scholar
  • 26 Henderson M. E. K., Duff R. B.. The release of metallic and silicate ions from minerals, rocks, and soils by fungal activity.  Journal of Soil Science. (1963);  14 236-246
    PubMedSearch in Google Scholar
  • 27 Hinsinger P., Jaillard B., Dufey J. E.. Rapid weathering of a trioctahedral mica by the roots of ryegrass.  Soil Science Society of America Journal. (1992);  56 977-982
    PubMedSearch in Google Scholar
  • 28 Hinsinger P., Gilkes R. J.. Root-induced irreversible transformation of trioctahedral mica on the rhizosphere of rape.  Journal of Soil Science. (1993);  44 535-545
    PubMedSearch in Google Scholar
  • 29 Hinsinger P., Gilkes R. J.. Root-induced dissolution of phosphate rock in the rhizosphere of lupines grown in alkaline soil.  Australian Journal of Soil Research. (1995);  33 477-489
    CrossrefPubMedSearch in Google Scholar
  • 30 Hirsch P., Eckhardt F. E. W., Palmer  Jr. R. J.. Methods for the study of rock-inhabiting microorganisms - A mini review.  Journal of Microbiology Methods. (1995 a);  23 143-167
    PubMedSearch in Google Scholar
  • 31 Hirsch P., Eckhardt F. E. W., Palmer  Jr. R. J.. Fungi active in weathering of rock and stone monuments.  Canadian Journal of Botany. (1995 b);  73 (Suppl. 1) S1384-S1390
    PubMedSearch in Google Scholar
  • 32 Holguin G., Guzman M. A., Bashan Y.. Two new nitrogen-fixing bacteria from the rhizosphere of mangroves trees, isolation, identification and in vitro interaction with rhizosphere Staphylococcus sp.  FEMS Microbiology Ecology. (1992);  101 207-216
    CrossrefPubMedSearch in Google Scholar
  • 33 Illmer P., Schinner F.. Solubilization of inorganic calcium phosphate-solubilization mechanisms.  Soil Biology and Biochemistry. (1995);  27 257-263
    CrossrefPubMedSearch in Google Scholar
  • 34 Illmer P., Barbato A., Schinner F.. Solubilization of hardy-soluble AIPO4 with P-solubilizing microorganisms.  Soil Biology and Biochemistry. (1995);  27 265-270
    CrossrefPubMedSearch in Google Scholar
  • 35 Jackson M. L.. Soil Chemical Analysis. Englewood Cliffs, NJ; Prentice-Hall, Inc (1958)
    Search in Google Scholar
  • 36 Johnston C. G., Vestal J. R.. Biogeochemistry of oxalate in the Antarctic cryptoendolithic lichen-dominated community.  Microbial Ecology. (1993);  25 305-319
    PubMedSearch in Google Scholar
  • 37 King E. O., Ward M. K., Raney D. E.. Two simple media for the demonstration of pyocyanin and fluorescin.  Journal of Laboratory and Clinical Medicine. (1954);  44 301-307
    PubMedSearch in Google Scholar
  • 38 Kingston H. M.. EPA Method 3015 Microwave Assisted Acid Digestion of Aqueous Samples and Extracts. Pittsburgh, PA, USA; Dusquesne University (1994)
    Search in Google Scholar
  • 39 Krumbein W. E., Jens K.. Biogenic rock varnishes of the Negev Desert (Israel), an ecological study of iron and manganese transformation by cyanobacteria and fungi.  Oecologia (Berlin). (1981);  50 25-38
    CrossrefPubMedSearch in Google Scholar
  • 40 Levanony H., Bashan Y., Romano B., Klein E.. Ultrastructural localization and identification of Azospirillum brasilense Cd on and within wheat root by immuno-gold labeling.  Plant and Soil. (1989);  117 207-218
    PubMedSearch in Google Scholar
  • 41 Leyval C., Laheurte F., Belgy G., Berthelin J.. Weathering of micas in the rhizosphere of maize, pine and beech seedlings influenced by mycorrhizal and bacterial inoculation.  Symbiosis. (1990);  9 105-109
    PubMedSearch in Google Scholar
  • 42 Lynch J. M., Whipps J. M.. Substrate flow in the rhizosphere.  Plant and Soil. (1990);  129 1-10
    CrossrefPubMedSearch in Google Scholar
  • 43 Meyer J. R., Lindrman R. G.. Response of subterranean clover to dual inoculation with vesicular-arbuscular mycorrhizal fungi and a plant growth-promoting bacterium, Pseudomonas putida. .  Soil Biology and Biochemistry. (1986);  18 185-190
    CrossrefPubMedSearch in Google Scholar
  • 44 Osburn R. M., McCain A. H., Schroth M. N.. Biocontrol of Pythium ultimum damping off of sugar beets with rhizosphere bacteria (Abstract).  Phytopathology. (1983);  73 961
    PubMedSearch in Google Scholar
  • 45 Palmer  Jr. R. J., Siebert J., Hirsch P.. Biomass and organic acids in sandstone of a weathering building production by bacterial and fungal isolates.  Microbial Ecology. (1991);  21 253-266
    PubMedSearch in Google Scholar
  • 46 Pikoskaya R. I.. Mobilization of phosphates in soil in relation with vital activity of some microbial species [In Russian].  Mikrobiologiya. (1948);  17 362-370
    PubMedSearch in Google Scholar
  • 47 Puente M. E., Bashan Y.. Effect of inoculation with Azospirillum brasilense strains on the germination and seedlings growth of the giant columnar cardon cactus (Pachycereus pringlei). .  Symbiosis. (1993);  15 49-60
    PubMedSearch in Google Scholar
  • 48 Puente M. E., Bashan Y.. The desert epiphyte Tillandsia recurvata harbors the nitrogen-fixing bacterium Pseudomonas stutzeri. .  Canadian Journal of Botany. (1994);  72 406-408
    PubMedSearch in Google Scholar
  • 49 Puente M. E., Holguin G., Glick B. R., Bashan Y.. Root-surface colonization of black mangrove seedlings by Azospirillum halopraeferens and Azospirillum brasilense in seawater.  FEMS Microbiology Ecology. (1999);  29 283-292
    CrossrefPubMedSearch in Google Scholar
  • 50 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 Biology. (2004);  DOI: 10.1055/s-2004-821101
    PubMedSearch in Google Scholar
  • 51 Rennie R. J.. A single medium for the isolation of acetylene-reducing (dinitrogen-fixing) bacteria from soils.  Canadian Journal of Microbiology. (1981);  27 8-14
    PubMedSearch in Google Scholar
  • 52 Söderström B. E.. Vital staining of fungi in pure cultures and in soil with fluorescein diacetate.  Soil Biology and Biochemistry. (1977);  9 59-63
    CrossrefPubMedSearch in Google Scholar
  • 53 Sorensen J.. The rhizosphere as a habitat for soil microorganisms. van Elsas, J. D., Trevors, J. T., and Wellington, E. M. H., eds. Modern Soil Microbiology. New York; Marcel Dekker, Inc. (1997): 21-45
    Search in Google Scholar
  • 54 Sun H. J., Friedmann E. I.. Growth on geological time scales in the Antarctic cryptoendolithic microbial community.  Geomicrobiology Journal. (1999);  16 193-202
    CrossrefPubMedSearch in Google Scholar
  • 55 Vazquez P., Holguin G., Puente M. E., Lopez-Cortes A., Bashan Y.. Phosphate-solubilizing microorganisms associated with the rhizosphere of mangroves growing in a semiarid coastal lagoon.  Biology and Fertility of Soils. (2000);  30 460-468
    CrossrefPubMedSearch in Google Scholar
  • 56 Verges V.. Solution and associated features of limestone fragments in a calcareous soil (Lithic Calcixeroll) from southern France.  Geoderma. (1985);  36 109-122
    CrossrefPubMedSearch in Google Scholar

Y. Bashan

Environmental Microbiology Group
Center for Biological Research of the Northwest (CIB)

P.O. Box 128

La Paz, B.C.S. 23000

Mexico

Email: bashan@cibnor.mx

Section Editor: M. C. Ball