Usage of ferrum (ІІІ) and manganese (IV) ions as electron acceptors by Desulfuromonas sp. bacteria

  • O. M. Moroz Ivan Franko National University of Lviv
  • S. O. Hnatush Ivan Franko National University of Lviv
  • C. I. Bohoslavets Ivan Franko National University of Lviv
  • G. V. Yavorska Ivan Franko National University of Lviv
  • N. V. Truchym Ivan Franko National University of Lviv
Keywords: sulphur reducing bacteria, anaerobic respiration, heavy metals

Abstract

The toxicity of metal ions to microorganisms, in particular at high concentrations, is one of the main impediments to their usage in remediation technologies. The purpose of this work is to analyze the possibility of usage by bacteria of the Desulfuromonas genus, isolated by us from Yavorivske Lake, of ferrum (ІІІ) and manganese (IV) ions at concentrations in the medium of 1,74–10,41 mM as electron acceptors of anaerobic respiration to assesss resistance of sulphur reducing bacteria strains to heavy metal compounds. Cells of Desulfuromonas acetoxidans ІМV V-7384, Desulfuromonas sp. Yavor-5 and Desulfuromonas sp. Yavor-7 were cultivated for 10 days at 30 °C under anaerobic conditions in Kravtsov-Sorokin’s medium without sulphate ions, sulphur, with cysteine as the sulphur source (0.2 g/l) and sodium lactate or citrate as the electron donor (17.86 g/l), in which were added sterile 1 M solutions of C6H5O7Fe and C4H4O4 (control) and also weights of MnO2 to their terminal concentrations 1.74, 3.47, 5.21, 6.94, 10.41 mM. Biomass was determined by the turbidimetric method. In the culture liquid the presence of Fe3+ and Mn4+ were qualitatively determined, and the content of Fe2+ in reaction with о-phenanthroline was determined quantitatively. It was established that sulphur reducing bacteria used with different intensity ferrum (ІІІ) and manganese (IV) ions as electron acceptors during the process of anaerobic respiration at concentrations of 1.74–10.41 mM C6H5O7Fe and MnO2 in the medium, which demonstrated the important role of the investigated microorganisms in reductive detoxication of natural and technogenic media from oxidized forms of transitional heavy metals. An insignificant difference in biomass accumulation during usage of 5.21–10.41 mM ferrum (ІІІ) ions and fumarate is caused by toxicity of the metal ions to cells since the high redox potential of the Fe(III)/Fe(ІІ) pair with increase in concentrations of electron acceptors in the medium did not lead to increase in the biomass accumulation level. The greatest biomass of the bacteria accumulated on the 8–10th days in the medium with the lowest concentration of C6H5O7Fe – 1.74 mM (up to 2.77 g/l), and the lowest biomass – with highest concentration – 10.41 mM (up to 2.41 g/l). After 10 days of cultivation the bacteria of all strains had fully used the ferrum (ІІІ) ions present in the medium. A biomass yield almost twice as low was revealed after manganese (IV) oxide was used by bacteria compared with its use of ferrum (ІІІ) citrate and fumarate at all studied concentrations of electron acceptors in the medium. The highest biomass of bacteria accumulated in the medium with the lowest MnO2 content – 1.74 mM (up to 1.35 g/l), and the lowest biomass in the medium with the highest content – 10.41 mM (up to 1.15 g/l). After 10 days of cultivation bacteria of all strains had not fully restored the manganese (IV) ions present in the medium. The greatest biomass compared with other strains after growth in medium with different C6H5O7Fe and MnO2 contents was accumulated by the strain Desulfuromonas sp. Yavor-7. Since sulphur reducing bacteria strains proved to be resistant to Fe3+ and Mn4+ high concentrations (up to10.41 mM) they can be successfully used in technologies of environmenal remediation from sulphur and heavy metal compounds. 

References

Aklujkar, M., Coppi, M.V., Leang, C., Kim, B.C., Chavan, M.A., Perpetua, L.A., Giloteaux, L., Liu, A., Holmes, D.E., 2013. Proteins involved in electron transfer to Fe (III) and Mn (IV) oxides by Geobacter sulfurreducens and Geobacter uraniireducens. Microbiology 159(3), 515–535.

Bilyy, O.I. Vasyliv, O.M., Hnatush, S.O., 2014. The anode biocatalyst with simultaneous transition metals pollution control. Technology and application of microbial fuel cells. InTech, Rijeka, Croatia.

Cologgi, D.L., Lampa-Pastirk, S., Speers, A.M., Kelly, S.D., Reguera, G., 2011. Extracellular reduction of uranium via Geobacter conductive pili as a protective cellular mechanism. Proc. Natl. Acad. Sci. USA 108, 15248–15252.

Dey, U., Chatterjee, S., Mondal, N.K., 2016. Isolation and characterization of arsenic-resistant bacteria and possible application in bioremediation. Biotechnology Reports 10, 1–7.

Fitzgeralda, L.A., Petersenb, E.R., Learyc, D.H., Nadeaud, L.J., Sotoe, C.M., Rayf, R.I., Littlef, B.J., Ringeisena, B.R., Johnsond, G.R., Vorae, G.J., Biffingera, J.C., 2013. Shewanella frigidimarina microbial fuel cells and the influence of divalent cations on current output. Biosens. Bioelectron. 40(1), 102–109.

Fonseca, B.M., Paquete, C.M., Neto, S.E., Pacheco, I., Soares, C.M., Louro, R.O., 2013. Mind the gap: Cytochrome interactions reveal electron pathways across the periplasm of Shewanella oneidensis MR-1. Biochem. J. 449(1), 101–108.

Gescher, J., Kappler, A., 2013. Microbial metal respiration: From geochemistry to potential applications. Springer-Verlag, Berlin Heidelberg.

Gralnick, J.A., 2012. On conducting electron traffic across the periplasm. Biochm. Soc. Trans. 40(6), 1178–1180.

Gudz, S.P., Peretiatko, T.B., Moroz, O.M., Hnatush, S.O., Klym, I.R., 2011. Rehulyuvannya rivnya sul’fativ, sirkovodnyu ta vazhkykh metaliv u tekhnohennykh vodoymakh sulfatvidnovljuval’nymy bakterijamy [Regulation of sulfates, hydrogen sulfide and hard metals level in technogenic reservoirs by sulfate reducing bacteria]. Microbiologichny Zhurnal 73(2), 33–38 (in Ukrainian).

Gudz, S.P., Нnatush, S.O., Moroz, O.M., Peretiatko, T.B., Vasyliv, O.M., 2013. Svidotstvo pro deponuvannya shtamu bakteriy Desulfuromonas acetoxidans Ya-2006 u Depozytariyi Instytutu mikrobiolohiyi i virusolohiyi im. D. K. Zabolotnoho NAN Ukrayiny z nadannyam reyestratsiynoho nomeru IMV V-7384 [Certificate of deposition of bacteria Desulfuromonas acetoxidans Ya-2006 strain in the Depository of D.K. Zabolotny Institute of Microbiology and Virology of the NAS of Ukraine with appropriation of registration number IMV V-7384] (in Ukrainian).

Gudz, S.P., Нnatush, S.O., Yavorska, G.V., Bilinska, I.S., Borsukevych, B.M., 2014. Praktykum z mikrobiologii [Workshop on microbiology]. Lviv. Nac. Univ. imeni Ivana Franka. Ser. Biol. Stud., Lviv (in Ukrainian).

Harris, D.S., 2003. Quantitative chemical analysis. W.H. Free-man, New York.

Iwahori, K., Watanabe, J., Tani, Y., Seyama, H., Miyata, N., 2014. Removal of heavy metal cations by biogenic magnetite nanoparticles produced in Fe(III)-reducing microbial enrichment cultures. J. Biosci. Bioeng. 117(3), 333–335.

Karavajko, G.I., Kuznetsov, S.I., Golomzyk, A.I., 1972. Rol’ mikroorganyzmov v vyshhelachyvanyy metallov iz rud [The role of microorganisms in release of metals from minerals]. Nauka, Moscow (in Russian).

Kiran, M.G., Pakshirajan, K., Das, G., 2016. Heavy metal removal from multicomponent system by sulfate reducing bacteria: Mechanism and cell surface characterization. J. Hazard. Mater. In press.

Kreshkov, A.P., 1961. Osnovy analytycheskoj hіmyy [Basis of аnalytical chemistry]. Goshimizdat, Moscow (in Russian).

Lengeler, J., Drevs, G., Schlegel, G., 2005. Sovremennaja mikrobyologyja: Prokaryoty [Modern Microbiology: Prokaryotes]. Mir, Moscow (in Russian).

Limcharoensuk, T., Sooksawat, N., Sumarnrote, A., Awutpet, T., Kruatrachue, M., Pokethitiyook, P., Auesukaree, C., 2015. Bioaccumulation and biosorption of Cd2+ and Zn2+ by bacteria isolated from a zinc mine in Thailand. Ecotox. En-viron. Safe. 122, 322–330.

Liu, L., Lee, D.-J., Wang, A., Ren, N., Su, A., Lai, J.-Y., 2016. Isolation of Fe (III)-reducing bacterium, Citrobacter sp. LAR-1, for startup of microbial fuel cell. Int. J. Hydrogen Energ. 41(7), 4498–4503.

Lovley, D., 2006. Dissimilatory Fe (III)- and Mn (IV)-reducing pro¬karyotes. The Procaryotes. Springer-Verlag, LLC, New York.

Lovley, D.R., 1995. Microbial reduction of iron, manganese and other metals. Adv. Agron. 54, 175–231.

Lovley, D.R., Giovannoni, S.J., White, D.C., Champine, J.E., Phillips, E.J. P., Gorby, Y.A., Goodwin, S., 1993. Geobacter metallireducens gen. nov. sp. nov., a microorganism capable of coupling the complete oxidation of organic compounds to the reduction of iron and other metals. Arch. Microbiol. 159, 336–344.

Mardanov, A.V., Slododkina, G.B., Slobodkin, A.I., Beletsky, A.V., Gavrilov, S.N., Kublanov, I.V., Bonch-Osmolovskaya, E.A., Skryabin, K.G., Ravin, N.V., 2015. The Geoglobus acetivorans genome: Fe (III) reduction, acetate utilization, autotrophic growth, and degradation of aromatic compounds in a hyperthermophilic archaeon. Appl. Environ. Microbiol. 81(3), 1003–1012.

Moroz, O., Gul’, N., Galushka, A., Zvir, G., Borsukevych, B., 2014. Vykorystannja riznyh akceptoriv elektroniv bakterijamy Desulfuromonas sp., vydilenymy z ozera Javorivs’ke [Different electron acceptors usage by bacteria of Desulfuromonas sp. isolated from Yavorivske Lake]. Visn. Lviv. Univ. Ser. Biol. 65, 322–334 (in Ukrainian).

Moroz, O.M., 2013. Utvorennja gidrogen sul’fidu sirkovidnovljuval’nymy bakterijamy za vplyvu solej vazhkyh metaliv [Hydrogen sulfide production by sulfur reducing bacteria under the influence of hard metals]. Visn. Lviv. Univ. Ser. Biol. 61, 154–165 (in Ukrainian).

Moroz, O.M., Peretiatko, T.B., Klym, I.R., Borsukevych, B.M., Yavorska, G.V., Kulachkovsky, A.R., 2013. Sirkovidnovljuval’ni bakterii’ ozera Javorivs’ke: Dejaki morfologichni, kul’tural’ni i fiziologichni osoblyvosti [Sulfur reducing bacteria from Yavorivske Lake: Some morphological, cultural and physiological peculiarities]. Nauk. Visn. Uzhgorod. Univ. Ser. Biol. 35, 34–41 (in Ukrainian).

Moroz, O.M., Yavorska, G.V., Muravel’, N.O., Klym, I.R., 2012. Vidnovlennja ferumu (ІІІ) sulfatvidnovljuval’nymy i sirkovidnovljuval’nymy bakterijamy [Reduction of ferrum (III) by sulfate reducing and sulfur reducing bacteria]. Studia Biologica 6(2), 161–172 (in Ukrainian).

Mustapha, M.U., Halimoon, N., 2015. Screening and isolation of heavy metal tolerant bacteria in industrial effluent. Procedia Environ. Sci. 30, 33–37.

Qian, X., Mester, T., Morgado, L., Arakawa, T., Sharma, M.L., Inoue, K., Joseph, C., Salgueiro, C.A., Maroney, M.J., Lovley, D.R., 2011. Biochemical characterization of purified OmcS, a c-type cytochrome required for insoluble Fe (III) reduction in Geobacter sulfurreducens. Biochim. Biophys. Acta 1807(4), 404–412.

Rabus, R., Venceslau, S.S., Wöhlbrand, L., Voordouw, G., Wall, J.D., Pereira, I.A.C., 2015. A post-genomic view of the ecophysiology, catabolism and biotechnological relevance of sulphate-reducing prokaryotes. Chapter 2. Adv. Microb. Physiol. 66, 55–321.

Richter, K., Schicklberger, M., Gescher, J., 2012. Dissimilatory reduction of extracellular electron acceptors in anaerobic respiration. Appl. Environ. Microbiol. 78(4), 913–921.

Roden, E.E., Lovley, D.R., 1993. Dissimilatory Fe (III) reduction by the marine microorganism Desulfuromonas acetoxidans. Appl. Environ. Microbiol. 59, 734–742.

Schicklberger, M., Bucking, C., Schuetz, B., Heide, H., Gescher, J., 2011. Involvement of the Shewanella oneidensis decaheme cytochrome MtrA in the periplasmic stability of the beta-barrel protein MtrB. Appl. Environ. Microbiol. 77, 1520–1523.

Si, Y., Zou, Y., Liu, X., Si, X., Mao, J., 2015. Mercury methylation coupled to iron reduction by dissimilatory iron-reducing bacteria. Chemosphere 122, 206–212.

Smirnova, G.F., Podgorsky, V.S., 2013. Vosstanovlenie hromatov Pseudomonas sp. sht. 10 v prisutstvii nekotoryh tjazhjolyh metallov i al’ternativnyh akceptorov jelektronov [Chromates reducing by Pseudomonas sp. str. 10 in presence of some heavy metals and alternative electron acceptors]. Microbiologichny Zhurnal 75(4), 8–12 (in Russian).

Tebo, B.M., 1995. Metal precipitation by marine bacteria: Potential for biotechnological applications. Genetic engineering – principles and methods. Plenum Press, New York.

Tebo, B.M., Obraztsova, A.Y., 1998. Sulfate-reducing bacterium grows with Cr (VI), U (VI), Mn (IV), and Fe (III) as electron acceptors. FEMS Microbiol. Lett. 162, 193–198.

Tremblay, P.-L., Summers, Z.M., Glaven, R.H., Nevin, K.P., Zengler, K., Barrett, C.L., Qiu, Y., Palsson, B.O., Lovley, D.R., 2011. A c-type cytochrome and a transcriptional regulator responsible for enhanced extracellular electron transfer in Geobacter sulfurreducens revealed by adaptive evolution. Environ. Microbiol. 13(1), 13–23.

Tsvetkova, N.M., Pakhomov, O.Y., Serdyuk, S.M., Yakyba, M.S., 2016. Biologichne riznomanittja Ukrajiny. Dnipropetrovs'ka oblast'. Grunty. Metaly u gruntah [Bіological diversity of Ukraine. The Dnipropetrovsk region. Soils. Metalls in the soils]. Lira, Dnipropetrovsk (in Ukrainian).

Viti, C., Marchi, E., Decorosi, F., Giovannetti, L., 2014. Molecular mechanisms of Cr (VI) resistance in bacteria and fungi. FEMS Microbiol. Rev. 38(4), 633–659.

Wang, Q., Ding, D., Hu, E., Yu, R., Qiu, G., 2008. Removal of SO42–, uranium and other heavy metal ions from simulated solution by sulfate reducing bacteria. T. Nonferr. Metal. Soc. 18(6), 1529–1532.

Wang, W., Feng, Y., Tang, X., Li, H., Du, Z., Yi, A., Zhang, X., 2015. Enhanced U(VI) bioreduction by alginate-immobilized uranium-reducing bacteria in the presence of carbon nanotubes and anthraquinone-2,6-disulfonate. J. Environ. Sci. 31, 68–73.

Wilkins, M.J., Callister, S.J., Miletto, M., Williams, K.H., Nicora, C.D., Lovley, D.R., Long, P.E., Lipton, M.S., 2011. Development of a biomarker for Geobacter activity and strain composition; proteogenomic analysis of the citrate synthase protein during bioremediation of U (VI). Microb. Biotechnol. 4(1), 55–63.

Zhuang, K., Ma, E., Lovley, D.R., Mahadevan, R., 2012. The design of long-term effective uranium bioremediation strategy using a community metabolic model. Biotechnol. Bioeng. 109(10), 2475–2483.

Published
2016-03-07
Section
Articles

Most read articles by the same author(s)