Skip to main content
SpringerLink
Log in

Evidence for the interference of aluminum with bacterial porphyrin biosynthesis

  • Research Papers
  • Published:
Biometals Aims and scope Submit manuscript

Abstract

Aluminum (0.74 mm) was found to retard bacterial growth, and enhance porphyrin formation and excretion in Arthrobacter aurescens RS-2. Coproporphyrin III was shown to be the main porphyrin excreted by aluminum-exposed A. aurescens RS-2 cultures and by RS-2 cultures grown under anoxic conditions. Synthesis and excretion of porphyrins in A. aurescens RS-2 increased in a dose-dependent manner when the bacteria were exposed to increasing aluminum concentrations. Incubation of A. aurescens RS-2 with δ-aminolevulinic acid (δ-ALA, 1.2 mm) brought about the intense formation and excretion of porphyrins by the cells, in the presence or absence of aluminum. δ-ALA slightly enhanced the toxicity of aluminum towards RS-2 bacteria. Furthermore, the intracellular concentration of heme was reduced by 63.9 ± 8.67% in aluminum-exposed RS-2 bacteria when compared with control cultures. The results are discussed in light of the recent finding concerning aluminum toxicity and porphyrin biosynthesis in microorganisms.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Avissar YJ, Nadler KD. 1978 Stimulation of tetrapyrrole formation in Rhizobium japonicum by restricted aeration. J Bacteriol 135, 782–789.

    Google Scholar 

  • Bevins M, Yang CM, Markwell J. 1992 Characterization of chlorophyll-deficient mutant of sweetclover (Melilotus alba). Plant Physiol Biochem 30, 327–331.

    Google Scholar 

  • Bia MJ, Cooper K, Schnall S, Duffy T, Hendler E, Malluche H, Solomon L. 1989 Aluminum induced anemia: pathogenesis and treatment in patients on chronic hemodialysis. Kidney Int 36, 852–858.

    Google Scholar 

  • Biel AJ. 1992 Oxygen-regulated steps in the Rhodobacter capsulatus tetrapyrrole biosynthetic pathway. J Bacteriol 174, 5272–5274.

    Google Scholar 

  • Biel SW, Biel AJ. 1990 Isolation of a Rhodobacter capsulatus mutant that lacks c-type cytochromes and excretes porphyrins. J Bacteriol 172, 1321–1326.

    Google Scholar 

  • Buchet JP, Lauwerys R, Hassoun A, et al. 1987 Effect of aluminum on porphyrin metabolism in hemodialyzed patients. Nephron 46, 360–363.

    Google Scholar 

  • Burnham BF, Lascelles J. 1963 Control of porphyrin biosynthesis through a negative-feedback mechanism. Biochem J 87, 462–472.

    Google Scholar 

  • Cavaleiro JAS, Kenner GW, Smith KM. 1973 Biosynthetic intermediates between coproporphyrinogen-III and protoporphyrin IX. JCS Chem Commun 183–184.

  • Clesceri LS, Greenberg AE, Trussell RR, eds 1989 Standard Methods for the Examination of Water and Wastewater, 17th edn. Washington: American Public Health Association, section 3111D, pp. 3–25.

    Google Scholar 

  • Dailey HA. 1982 Purification and characterization of membrane-bound ferrochelatase from Rhodopseudomonas spheroides. J Biol Chem 257, 14714–14718.

    Google Scholar 

  • Dolphin D. 1978 The Porphyrins. New York: Academic Press.

    Google Scholar 

  • Driscoll CT, Schecher WD. 1990 The chemistry of aluminum in the environment. Environ Geochem Health 12, 28–49.

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  • Hughes MN, Poole RK. 1989 Metals and Microorganisms. London: Chapman & Hall.

    Google Scholar 

  • Jackson-Moss CA, Duncan JR. 1991 The effect of aluminim on anaerobic digestion. Biotech Lett 13, 143–148.

    CAS  PubMed  Google Scholar 

  • Javor GT, Febre EF. 1992 Enzymatic basis of thiol-stimulated secretion of porphyrins by Escherichia coli. J Bacteriol 174, 1072–1075.

    Google Scholar 

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

    Google Scholar 

  • Kok CJ, Meesters HWG, Kempers AJ. 1990 Decomposition rate, chemical composition and nutrient recycling of Nymphaea alba L. floating leaf blade detritus as influenced by pH, alkalinity and aluminum in laboratory experiments. Aqua Bot 37, 215–227.

    Google Scholar 

  • Lim CK, Peters TJ. 1984 Urine and faecal porphyrin profiles by reverse-phase high performance liquid chromatography in the porphyrias. Clin Chem Acta 139, 55–63.

    Google Scholar 

  • Lindemann J, Holtkamp E, Herrmann R. 1990 The impact of aluminum on green algae isolated from two hydrochemically different headwater streams, Bavaria, Germany. Environ Pollut 67, 61–77.

    Google Scholar 

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

    Google Scholar 

  • McGonigle RJ, Parsons V. 1985 Aluninium-induced anaemia in haemodialysis patients. Nephron 39, 1–9.

    Google Scholar 

  • Middleton KS, Gunner HB. 1968 Porphyrin production by Arthrobacter globiformis. Can J Microbiol 14, 1095–1103.

    Google Scholar 

  • Mori M, Sano S. 1972 Studies on the formation of protoporphyrin IX by anaerobic bacteria. Biochem Biophys Acta 264, 252–262.

    Google Scholar 

  • Morrison JR. 1967 Fluorometric micro-determination of heme protein. Anal Chem 37, 1124–1126.

    Google Scholar 

  • Mulder J, van Grinsven JJM, van Breemen. 1987 Impacts of acid atmospheric deposition on woodland soils in the Netherlands: III. Aluminum chemistry. Soil Sci Soc Am J 51, 1640–1646.

    Google Scholar 

  • Neal C, Reynolds B, Smith CJ, et al. 1992 The impact of conifer harvesting on stream water pH, alkalinity and aluminium concentrations for the british uplands: an example for an acidic and acid sensitive catchment in mid-Wales. Sci Total Environ 126, 75–87.

    Google Scholar 

  • Nir U, Ladan H, Malik Z, Nitzan Y. 1991 In vivo effects of porphyrins on bacterial DNA. J Photochem Photobiol B: Biol 11, 295–306.

    Google Scholar 

  • Nyholm E. 1981 Evidence of involvment of aluminum in causation of defective formation of eggshells and of impaired breeding in wildpasserine birds. Environ Res 26, 363–371.

    Google Scholar 

  • Octive JC, Wood M, Johnson AC. 1991 mutagenic effects of aluminium. Mutat Res 264, 135–137.

    Google Scholar 

  • Oelze J. 1992 Light and oxygen regulation of the synthesis of bacteriochlorophylls a and c in Chloroflexus aurantiacus. J Bacteriol 174, 5021s-5026.

    Google Scholar 

  • Ravishanker CH, Padmanaban G. 1985 Regulation of cytochrom P-450 gene expression. J Biol Chem 260, 1588–1592.

    Google Scholar 

  • Rosenlof K, Fyhrquist F, Tenhunen R. 1990 Erythropoietin, aluminium, and anaemia in patients on haemodialysis. Lancet 335, 247–249.

    Google Scholar 

  • Rosseland BO, Eldhuset TD, Staurnes M. 1990 Environmental effects of aluminum. Environ Geochem Health 12(1/2), 17–27.

    Google Scholar 

  • Scharf R, Zimmels Y, Kimchie S. 1993 Metal induced extracellular protein excretion in Arthrobacter aurescens. FEMS Microbiol Lett 109, 139–144.

    Google Scholar 

  • Schoenfeld N, Mamet R. 1991 High-performance liquid chromatographic detection of pitfalls in porphobilinogen deaminase determination. J Chromatogr 570, 51–64.

    Google Scholar 

  • Sitjes J, Ysern P, Barbe J, Llagostera. 1992 Induction of ribonucleoside diphosphate reductase gene transcription by chemicals in Escherichia coli. Mutagenesis 7, 47–49.

    Google Scholar 

  • Smith SG, Belcher RV. 1974 Distribution of some intermediates of the haem biosynthesis. Enzyme 17, 1–10.

    Google Scholar 

  • Thornton FC, Davey CB. 1983 Acid tolerance of Rhizobium trifolii in culture media. Soil Sci Soc Am J 47, 496–501.

    Google Scholar 

  • Townsley PM, Neilands JB. The iron and porphyrin metabolism of Microccus lysodeikticus. J. Biol Chem 224, 695–705.

  • Urban-Grimal D, Labbe-Bois R. 1981 Genetic and biochemical characterization of mutants of Saccharomyces cerevisiae blocked in six different steps of heme biosynthesis. Mol Gen Gen 183, 85–92.

    Google Scholar 

  • Vierstra R, Haug A. 1978 The effect of Al3+ on the physical properties of membrane lipids in Thermoplasma acidophilum. Biochem Biophys Res Commun 84, 138–143.

    Google Scholar 

  • Wood M, Cooper JE. 1988 Acidity, aluminum and multiplication of Rhizobium trifolii: possible mechanisms of aluminum toxicity. Soil Biol Biochem 20, 95–99.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Environmental Engineering, Faculty of Civil Engineering Technion-Israel Institute of Technology, Haifa, Israel

    Ram Scharf, Yoram Zimmels & Shlomo Kimchie

  2. The Laboratory of Biochemical Pharmacology, Beilinson Medical Center, Petach-Tikva, Israel

    Rivka Mamet & Nili Schoenfeld

Authors
  1. Ram Scharf
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Rivka Mamet
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yoram Zimmels
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Shlomo Kimchie
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Nili Schoenfeld
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Scharf, R., Mamet, R., Zimmels, Y. et al. Evidence for the interference of aluminum with bacterial porphyrin biosynthesis. Biometals 7, 135–141 (1994). https://doi.org/10.1007/BF00140483

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00140483

Keywords

Search

Navigation