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Microbial interactions with aluminium

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Abstract

Although aluminium is the most abundant metal in the Earth's crust, it lacks biological functions and shows a low bioavailability. Acid rain, however, solubilizes aluminium to toxic levels. Most research on the biological effects of aluminium has been centred on the analysis of aluminium-tolerant plants as well as its possible relationship with neurological disorders in humans. Also, several studies have been reported concerning aluminium effects on microorganisms, with more interest directed to cyanobacteria, soil bacteria and mycorrhizal fungi. Competition with iron and magnesium, and binding to DNA, membranes or cell walls are considered the main toxic effects of aluminium in microbes.

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References

  • Appanna VD, Kepes M, Rochon P. 1994 Aluminum tolerance inPseudomonas fluorescens ATCC 13525: involvement of a gelatinous lipid-rich residue.FEMS Microbiol Lett 119, 295–302.

    Google Scholar 

  • Appanna VD, St Pierre M. 1994 Influence of phosphate on aluminum tolerance inPseudomonas fluorescens.FEMS Microbiol Lett 124, 327–332.

    Google Scholar 

  • Barea JM. 1991 Vesicular-arbuscular mycorrhizae as modifiers of soil fertility.Adv Soil Sci 15, 1–36.

    Google Scholar 

  • Belliveau BH, Starodub MG, Cotter C, Trevors JT. 1987 Metal resistance and accumulation in bacteria.Biotechnol Adv 5, 101–127.

    Google Scholar 

  • Bradley TJ, Parker MS. 1968 Binding of aluminium ions byStaphylococcus aureus 893.Experientia 24, 1175–1176.

    Google Scholar 

  • Brady DJ, Edwards DG, Asher CJ, Blamey FPC. 1993 Calcium amelioration toxicity effects on root hair development in soybean (Glycine max (L) Merr.).New Phytol 123, 531–538.

    Google Scholar 

  • Bruce RC, Warrell LA, Edwards DG, Bell LC. 1988 Effects of aluminum and calcium in the soil solution of acid soils on root elongation ofGlycine max cv. Forrest.J Agric Res 38, 319–338.

    Google Scholar 

  • Carvalho MM, Edwards DG, Asher CJ, Andrew CS. 1981 Aluminum toxicity, nodulation and growth ofStylosanthes species.Agron J 73, 261–265.

    Google Scholar 

  • Carvalho MM, Edwards DG, Asher CJ, Andrew CS. 1982 Effects of aluminum in nodulation of twoStylosanthes species grown in nutrient solution.Plant Soil 64, 141–152.

    Google Scholar 

  • Cervantes C, Gutiérrez-Corona F. 1994 Copper resistance mechanisms in bacteria and fungi.FEMS Microbiol Rev 14, 121–138.

    Google Scholar 

  • Cervantes C, Ji G, Ramirez JL, Silver S, 1994 Resistance to arsenic compounds in microorganisms.FEMS Microbiol Rev 14, 355–367.

    Google Scholar 

  • Cho SW, Joshi JG. 1989 Time-dependent inactivation of glucose-6 phosphate dehydrogenase from yeast by aluminum.Toxicol Lett 47, 215–219.

    Google Scholar 

  • Cooksey DA, Azad HR. 1992 Accumulation of copper and other metals by copper-resistant plant-pathogenic and saprophytic pseudomonads.Appl Environ Microbiol 58, 274–278.

    Google Scholar 

  • Davis WB, McCauley MJ, Byers BR. 1971 Iron requirements and aluminum sensitivity of hydroxamic requiring strain ofBacillus megaterium.J Bacteriol 105, 589–594.

    Google Scholar 

  • Driscoll CT. 1985 Aluminum in acidic surface waters: chemistry, transport effects.Environ Health Perspect 63, 93–104.

    Google Scholar 

  • El-Ayouty YM, Shaaban-Dessouki SA. 1992 Morphological and structural aberrations ofSphaeronostoc sp. induced by Al3+.Egypt J Microbiol 27, 281–290.

    Google Scholar 

  • Exley C, Birchall JD. 1992 The cellular toxicity of aluminium.J Theor Biol 159, 83–98.

    Google Scholar 

  • Foy CD, Chaney RL, Shite MC. 1978 The physiology of metal toxicity in plants.Annu Rev Plant Physiol 29, 1259–1261.

    Google Scholar 

  • Gagen CJ, Sharpe WE, Carline RF. 1993 Mortality of brook trout, mottled sculpins and slimy sculpins during acidic episodes.Trans Am Fish Soc 122, 616–628.

    Google Scholar 

  • Ganrot PO. 1986 Metabolism and possible health effects of aluminium.Environ Health Perspect 65, 363–441.

    Google Scholar 

  • Gascoyne DJ, Connor JA, Bull AT. 1991 Capacity of siderophore-producing alkalophilic bacteria to accumulate iron, gallium and aluminium.Appl Microbiol Biotechnol 36, 136–141.

    Google Scholar 

  • Gilmour CC. 1992 Effect of acid deposition on microbial processes in natural waters. In: Mitchell R, ed.Environmental Microbiology. New York: Wiley-Liss; 33–57.

    Google Scholar 

  • Graham PH. 1992 Stress tolerance inRhizobium andBradyrhizobium, and nodulation under adverse soil conditions.Can J Microbiol 38, 475–484.

    Google Scholar 

  • Guida L, Saidi Z, Hughes MN, Poole RK. 1991 Aluminum toxicity and binding toEscherichia coli.Arch Microbiol 156, 507–512.

    Google Scholar 

  • Guzzo A, Diorio C, DuBow MS. 1991 Transcription of theEscherichia coli fliC gene is regulated by metal ions.Appl Environ Microbiol 57, 2255–2259.

    Google Scholar 

  • Guzzo J, Guzzo A, DuBow MS. 1992 Characterization of the effects of aluminum on luciferase biosensors for the detection of ecotoxicity.Toxicol Lett 64/65, 687–693.

    Google Scholar 

  • Husaini Y, Rai LC. 1992 pH dependent aluminium toxicity toNostoc linckia: studies on phosphate uptake, alkaline and acid phosphatase activity, ATP content, photosynthesis and carbon fixation.J Plant Physiol 139, 703–707.

    Google Scholar 

  • Johnson AC, Wood M. 1990 DNA, a possible site of action of aluminum inRhizobium spp.Appl Environ Microbiol 56, 3629–3633.

    Google Scholar 

  • Jones D, Muehlchen A. 1994 Effects of the potentially toxic metals, aluminium, zinc and copper on ectomycorrhizal fungi.J Environ Sci Health (A) 29, 949–966.

    Google Scholar 

  • Joshi JG. 1990 Aluminum, a neurotoxin which affects diverse metabolic reactions.Biofactors 2, 163–169.

    Google Scholar 

  • Keyser HH, Munns DN. 1979 Tolerance of rhizobia to acidity, aluminum and phosphate.Soil Sci Soc Am J 43, 519–523.

    Google Scholar 

  • Kinraide TB, Ryan PR, Kochian LV. 1992 Interactive effects of Al3+, H+ and other cations on r elongation considered in terms of cell-surface electrical potential.Plant Physiol 99, 1461–1468

    Google Scholar 

  • Koslowsky SD, Boerner REJ. 1989 Interactive effects of aluminum phosphorus and mycorrhizae on growth and nutrient uptake ofPanicum virgatum L.Environ Pollut 61, 107–125.

    Google Scholar 

  • Lesueur D, Diem HG, Dianda M, LeRoux C. 1993 Selection ofNradyrhizobium strains and provenances ofAcacia mangium andFaiderbia albida: relationship with their tolerance to acidity and aluminum.Plant Soil 149, 159–166.

    Google Scholar 

  • Macdonald TL, Martin RB. 1988 Aluminium ion in biological systems.Trends Biochem Sci 13, 15–19.

    Google Scholar 

  • Madsen EL, Alexander M. 1985 Effects of chemical speciation on the mineralization of organic compounds by microorganisms.Appl Environ Microbiol 50, 342–349.

    Google Scholar 

  • Martin F, Rubini P, Cote R, Kottke I. 1994 Aluminum polyphosphate complexes in the mycorrhizal basidiomyceteLaccaria bicolor: a27Al nuclear magnetic resonance study.Planta 194, 241–246.

    Google Scholar 

  • Martin RB. 1986 The chemistry of aluminium as related to biology and medicine.Clin Chem 32, 1797–1806.

    Google Scholar 

  • Munns DN. 1986 Acid soil tolerance in legumes and rhizobia.Adv Plant Nutr 2, 63–91.

    Google Scholar 

  • Murphy HE, Edwards DG, Asher CJ. 1984 Effects of aluminum on nodulation and early growth of four tropical pasture legumes.Aust J Agric Res 32, 663–673.

    Google Scholar 

  • Myrold DD, Nason GE. 1992 Effect of acid rain on soil microbial processes. In: Mitchell R, ed.Environmental Microbiology. New York: Wiley-Liss; 59–81.

    Google Scholar 

  • Oleyedun OA, van Loon GW. 1994 Factors affecting uptake of aluminum by the fungusNeocosmospora vasinfecta. In:15th World Cong. of Soil Science, Acapulco, Mexico:4a; 45

    Google Scholar 

  • Paulus W, Bresinsky W. 1989 Soil fungi and other microorganisms. In: Schulze ED, Lange DL, Oren R, eds.Forest Decline and Air Pollution, Ecological Studies 77. New York: Springer-Verlag; 110–120.

    Google Scholar 

  • Pettersson A, Hällbom L, Bergman B. 1985a Physiological and structural responses of the cyanobacteriumAnabaena cylindrica to aluminium.Physiol Plant 63, 153–158.

    Google Scholar 

  • Pettersson A, Kunst L, Bergman B, Roomans GM. 1985b Accumulation of aluminium byAnabaena cylindrica in polyphosphate granules and cell walls: an X-ray energy-dispersive microanalysis study.J Gen Microbiol 131, 2545–2548.

    Google Scholar 

  • Pettersson A, Hällbom, Bergman B. 1986 Aluminium uptake byAnabaena cylindrica.J Gen Microbiol 132. 1771–1774.

    Google Scholar 

  • Richardson AE, Simpson RJ, Djordjevic MA, Rolfe BJ. 1988 Expression of nodulation genes inRhizobium leguminosarum bv.trifolii is affected by low pH and by Ca and Al ions.Appl Environ Microbiol 54, 2541–2548.

    Google Scholar 

  • Scharf R, Mamet R, Zimmels Y, Kimchie S, Schoenfeld N. 1994 Evidence for the interference of aluminum with bacterial porphyrin biosynthesis.BioMetals 7, 135–141.

    Google Scholar 

  • Schroeder JI. 1988 Transport properties of K+ channels in the plasma membrane ofVicia faba guard cells.J Gen Physiol 92, 667–683.

    Google Scholar 

  • Silver S. 1983 Bacterial interactions with mineral cations and anions: good ions and bad. In: Westbroek P, DeJong EW, eds.Biomineralization and Biological Metal Accumulation. Dordrecht: Reidel; 439–457.

    Google Scholar 

  • Silver S. 1994 Exploiting heavy metal resistance systems in bioremediation.Res Microbiol 145, 61–67.

    Google Scholar 

  • Silver S. Walderhaugh M. 1992 Gene regulation of plasmid- and chromosome-determined inorganic ion transport in bacteria.Microbiol Rev 56, 195–228.

    Google Scholar 

  • Slawson RM, van Dyke MI, Lee H, Trevors JT. 1992 Germanium and silver resistance, accumulation, and toxicity in microorganisms.Plasmid 27, 72–79.

    Google Scholar 

  • Stenson JAE, Svensson JE, Cronberg G. 1993 Changes and interactions in the pelargic community in acidified lakes in Sweden.Ambio 22, 277–282.

    Google Scholar 

  • Suhayda CG, Haug A. 1986 Organic acids reduce aluminum toxicity in maize root membranes.Physiol Plant 68, 189–195.

    Google Scholar 

  • The Merck Index. 1989 11th edn. Rahway, NJ: Merck & Co.; 320.

  • Thompson GW, Medve RJ. 1984 Effects of aluminum and manganese on the growth of ectomycorrhizal fungi.Appl Environ Microbiol 48, 556–560.

    Google Scholar 

  • Trevors JT. 1987 Copper resistance in bacteria.Microbiol Sci 4, 29–31.

    Google Scholar 

  • Trevors JT, Stratton GW, Gadd GM. 1986 Cadmium transport, resistance and toxicity in bacteria, algae, and fungi.Can J Microbiol 32, 447–464.

    Google Scholar 

  • Vargas AAT, Graham PH. 1988Phaseolus vulgaris cultivar andRhizobium strain variation in acid-pH tolerance and nodulation under acid conditions.Field Crops Res 19, 91–101.

    Google Scholar 

  • Vargas E, Gutiérrez S, Ambriz ME, Cervantes C. 1995 Chromosome-encoded inducible copper resistance inPseudomonas strains.Antonie van Leeuwenhoek,68, 225–229.

    Google Scholar 

  • Whelan AM, Alexander M. 1986 Effects of low pH and high Al, Mn and Fe levels on the survival ofRhizobium trifolii and the nodulation of subterranean clover.Plant Soil 92, 363–371.

    Google Scholar 

  • Wilkinson KJ, Campbell PGC. 1993 Aluminum bioconcentration at the gill surface of juvenile atlantic salmon in acidic media.Environ Toxicol Chem 12, 2083–2095.

    Google Scholar 

  • Wood M, Cooper JE, Bjourson AJ. 1988 Response ofLotus rhizobia to acidity and aluminum in liquid culture and in soil.Plant Soil 107, 227–231.

    Google Scholar 

  • Zambenedetti P, Tisato F, Corain B, Zatta PF. 1994 Reactivity of l(III) with membrane phospholipids: a NMR approach.BioMetals 7, 244–252.

    Google Scholar 

  • Zel J, Stevek J, Crne H, Schara M. 1993 Effects of aluminum on membrane fluidity of the mycorrhizal fungusAmanita muscaria.Physiol Plant 89, 172–176.

    Google Scholar 

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Piña, R.G., Cervantes, C. Microbial interactions with aluminium. Biometals 9, 311–316 (1996). https://doi.org/10.1007/BF00817932

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