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Arsenic metabolism in marine bacteria and yeast

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Abstract

Arsenic metabolism was studied for two marine microorganisms, a facultative anaerobic bacterium, Serratia marinorubra, and an obligately aerobic yeast, Rhodotorula rubra. Both were cultivated in media with (74As) arsenate (As V), and the products of arsenate metabolism were determined qualitatively. Both the bacterium and the yeast produced arsenite (AS III) and methylarsonic acid [CH3AsO(OH)2]. In addition to the foregoing, only the yeast produced dimethylarsinic acid (CH3)2AsO(OH) and volatile alkylarsines. In contrast, the bacterium growing anaerobically with cobalamine as a cofactor did not synthesize gaseous forms of arsenic such as methylarsines. Neither organism synthesized arsoniumphospholipids such as those produced by marine phytoplankton or terrestrial fungi. The yeast did not accumulate arsenite, but instead transported some of it into the culture medium and methylated the remainder first to methylarsonic acid and then to dimethylarsinic acid. Finally, the latter compound was methylated further and volatile alkylarsines were formed. In contrast, the bacterium retained all products of arsenate metabolism intracellularly. Both the bacterium and the yeast, therefore, converted relatively toxic arsenate, the most abundant arsenic compound in seawater, to products that were presumably less toxic.

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Literature Cited

  • Andreae, M. O.: Determination of arsenic species in natural waters. Analyt. Chem. 49, 820–823 (1977)

    Google Scholar 

  • Andreae, M. O.: Distribution and speciation of arsenic in natural waters and some marine algae. Deep-Sea Res. 25, 391–402 (1978)

    Google Scholar 

  • Barnes, H.: Nutrient elements. In: Treatise on marine ecology and paleoecology. Vol. 1. Ecology, pp 297–344. Ed. by J. W. Hedgpeth. New York: Geological Society of America 1957. (Mem. geol. Soc. Am. No. 67)

    Google Scholar 

  • Benson, A. A., J. A. Bassham, M. Calvin, T. C. Goodale, V. A. Haas and W. Stepka: The path of carbon in photosynthesis. V. Paper chromatography and radioautography of the products. J. Am. chem. Soc. 72, 1710–1718 (1950)

    Google Scholar 

  • Blum, J. J.: Phosphate uptake by phosphate-starved Euglena. J. gen. Physiol. 49, 1125–1137 (1966)

    Google Scholar 

  • Braman, R. S.: Arsenic in the environment. In: Arsenical pesticides. Symp. Ser. Am. chem. Soc. 18, 108–123 (1975)

  • Braman, R. S. and C. G. Foreback: Methylated forms of arsenic in the environment. Science, N.Y. 182, 1247–1249 (1973)

    Google Scholar 

  • Cerbon, J.: Arsenic lipid complex formation during the active transport of arsenate in yeast. J. Bact. 97, 658–662 (1969)

    Google Scholar 

  • Challenger, F.: Biological methylation. Chem. Rev. 36, 351–361 (1945)

    Google Scholar 

  • Challenger, F.: Biological methylation. Adv. Enzymol. 12, 429–491 (1951)

    Google Scholar 

  • Chambers, E. L. and A. H. Whiteley: Phosphate transport in fertilized sea urchin eggs. 1. Kinetic aspects. J. cell. Physiol. 68, 289–308 (1966)

    Google Scholar 

  • Cooney, R. V., R. O. Mumma and A. A. Benson: Arsoniumphospholipid in algae. Proc natn. Acad. Sci. U.S.A. 75, 4262–4264 (1978)

    Google Scholar 

  • Cox, D. P. and M. Alexander: Production of trimethylarsine gas from various arsenic compounds by three sewage fungi. Bull. envir. Contam. Toxicol. 9, 84–88 (1973)

    Google Scholar 

  • Difco Laboratories: Difco Manual, 9th ed. Detroit, Michigan: Difco Laboratories 1953

    Google Scholar 

  • Doudoroff, M., H. A. Barker and W. Z. Hassid: Studies with bacterial sucrose phosphorylase. III. Arsenolytic decomposition of sucrose and of glucose-1-phosphate. J. biol. Chem. 170, 147–150 (1947)

    Google Scholar 

  • Ferguson, J. F. and J. Gavis: A review of the arsenic cycle in natural waters. Wat. Res. 6, 1259–1274 (1972)

    Google Scholar 

  • Fluharty, A. L. and D. R. Sanadi: Evidence for a vicinal dithiol in oxidative phosphorylation. Proc. natn. Acad. Sci. U.S.A. 46, 608–616 (1960)

    Google Scholar 

  • Fluharty, A. L. and D. R. Sanadi: On the mechanism of oxidative phosphorylation. II. Effects of arsenite alone and in combination with 2, 3-dimercaptopropanol. J. biol. Chem. 236, 2772–2778 (1961)

    Google Scholar 

  • Fox, G. E., L. J. Magram, W. E. Black, R. S. Wolfe and C. R. Woese: Classification of methanogenic bacteria by 16 S ribosomal RNA. Proc natn. Acad. Sci. U.S.A. 74, 4537–4541 (1977)

    Google Scholar 

  • Hedges, R. W. and S. Bumberg: Resistance to arsenic compounds conferred by a plasmid transmissible between strains of Escherichia coli. J. Bact. 115, 459–460 (1973)

    Google Scholar 

  • Hirata, F., O. H. Viveros, E. J. Diliberto and J. Axelrod: Identification and properties of two methyltransferases in conversion of phosphotidylethanolamine to phosphotidylcholine. Proc. natn. Acad. Sci. U.S.A. 75, 1718–1721 (1978)

    Google Scholar 

  • Irgolic, K. J., E. A. Woolson, R. A. Stockton, R. D. Newman, N. R. Bottino, R. A. Zingaro, P. C. Kearny, R. A. Pyles, S. Maeda, W. J. McShane and E. R. Cox: Characterization of arsenic compounds formed by Daphnia magna and Tetraselmis chuii from inorganic arsenate. Envir. Hlth Perspectives 19, 61–66 (1977)

    Google Scholar 

  • Johnson, D. L.: Simultaneous determination of arsenate and phosphate in natural waters. Envir. Sci. Technol. 5, 411–414 (1971)

    Google Scholar 

  • Johnson, D. L.: Bacterial reduction of arsenate in seawater. Nature, Lond. 240, 44–45 (1972)

    Google Scholar 

  • Johnson, D. L. and R. S. Braman: The speciation of arsenic and the content of germanium and mercury in members of the Sargassum community. Deep-Sea Res. 22, 503–507 (1975)

    Google Scholar 

  • Johnson, D. L. and M. E. Q. Pilson: Spectrophotometric determination of arsenite, arsenate and phosphate in natural waters. Analyt. chim. Acta 58, 289–299 (1972a)

    Google Scholar 

  • Johnson, D. L. and M. E. Q. Pilson: Arsenoto in the western north Atlantic and adjacent regions. J. mar. Res. 30, 140–149 (1972b)

    Google Scholar 

  • Johnson, D. L. and M. E. Q. Pilson: The oxidation of arsenic in seawater. Envir Letters 8, 157–171 (1975)

    Google Scholar 

  • Kay, E. R. M.: Incorporation of radioarsenate into proteins and nucleic acids of the Ehrlich lettre Ascites carcinoma in vitro. Nature, Lond. 206, 371–373 (1965)

    Google Scholar 

  • Kreps, E. and N. Verjbinskaya: Seasonal changes in the phosphate and nitrate content and in hydrogen ion concentration in the Barents Sea. J. Cons. perm. int, Explor. Mer 5, 327–346 (1930)

    Google Scholar 

  • Lowenthal, D. H., M. E. Q. Pilson and R. H. Byrne: The determination of the apparent dissociation constants of arsenic acid in seawater. J. mar. Res. 35, 653–669 (1977)

    Google Scholar 

  • McBride, B. C. and R. S. Wolfe: Biosynthesis of dimethylarsine by Methanobacterium. Biochemistry (Am. chem. Soc.), Easton, Pa. 10, 4312–4317 (1971)

    Google Scholar 

  • Mitchell, R. A., B. F. Chang, C. H. Huang and E. G. DeMaster: Inhibition of mitochondrial energy-linked functions of arsenate. Evidence for a nonhydrolytic mode of inhibitor action. Biochemistry (Am. chem. Soc.), Easton, Pa. 10, 2049–2054 (1971)

    Google Scholar 

  • National Academy of Sciences: Medical and biological effects of environmental pollution. Arsenic, 332 pp. Washington, D. C.: U.S. National Academy of Sciences 1977

    Google Scholar 

  • Parris, G. E. and F. E. Brinkman: Reactions which relate to environmental mobility of arsenic and antimony. II. Oxidation of trimethylarsine and trimethylstibine. Envir. Sci. Technol. 10, 1128–1134 (1976)

    Google Scholar 

  • Feters, R. A.: Biochemistry of some toxic agents. I. Present state of knowledge of biochemical lesions induced by trivalent arsenical poisoning. Bull. Johns Hopkins Hosp. 97, 1–20 (1955)

    Google Scholar 

  • Raymont, J. E. G.: Plankton and productivity in the oceans, 660 pp. New York: Pergamon Press 1963

    Google Scholar 

  • Riley, P. J.: Plankton Studies. II. V. Regional summary. J. mar. Res. 4, 162–171 (1939)

    Google Scholar 

  • Rosenberg, H., R. G. Gerdes and K. Chegwidden: Two systems for the uptake of phosphate in Escherichia coli. J. Bact. 131, 505–511 (1977)

    Google Scholar 

  • Rothstein, A. and K. Donovan: Interactions of arsenate with the phosphate transporting system of yeast. J. gen. Physiol. 46, 1075–1085 (1963)

    Google Scholar 

  • Sanders, G. J. and H. L. Windom: The uptake and reduction of arsenic species by marine algae. Estuar. cstl mar. Sci. (In press). (1980)

  • Seiwell, H. R.: The annual organic production and nutrient concentration of phosphorus requirement in the tropical western north Pacific. J. Cons. perm. int. Explor. Mer 10, 20–32 (1935)

    Google Scholar 

  • Smith, H. W.: Arsenic resistance in Enterobacteria: its transmission by conjugation and by phage. J. gen. Microbiol. 109, 49–56 (1978)

    Google Scholar 

  • Stocken, L. A. and R. H. S. Thompsen: Reactions of British antilewisite with arsenic and other metals in living systems. Physiol. Rev. 29, 168–194 (1949)

    Google Scholar 

  • Sugawara, K., K. Terada, S. Kanamori, N. Kanamori and S. Okabe: On different distribution of calcium, strontium, iodine, arsenic and molybdenum in the northwestern Pacific, Indian and Antarctic Oceans. J. Earth Sci. 10, 34–50 (1962)

    Google Scholar 

  • Thomsen, H.: Hydrographic observations made during the Dana Expedition, 1928–1930. Dana Rep. 12, 1–46 (1937)

    Google Scholar 

  • Vallee, B. L., D. D. Ulmer and W. E. C. Wacker: Arsenic toxicology and biochemistry. A.M.A. Archs ind. Hlth 21, 132–151 (1960)

    Google Scholar 

  • Waslenchuk, G. D.: The budget and geochemistry of arsenic in a continental shelf environment. Mar. Chem. 7, 39–52 (1978)

    Google Scholar 

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Authors and Affiliations

  1. Scripps Institution of Oceanography, Mail Code A-008, 92093, La Jolla, California, USA

    F. V. Vidal & V. M. V. Vidal

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  1. F. V. Vidal
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  2. V. M. V. Vidal
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Communicated by N. D. Holland, La Jolla

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Vidal, F.V., Vidal, V.M.V. Arsenic metabolism in marine bacteria and yeast. Mar. Biol. 60, 1–7 (1980). https://doi.org/10.1007/BF00395600

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