Sulfidogenic and metal reducing activities of Desulfuromonas genus bacteria under the influence of copper chloride

Keywords: sulphur-reducing bacteria; hydrogen sulfide; copper; heavy metals.

Abstract

The selection of strains isolated from technogenically altered ecotopes and resistant to contamination, capable of metabolizing a wide range of pollutants is a task highly relevant for creation of new methods for environmental purification. Sulphur-reducing bacteria of the Desulfuromonas genus carry out dissimilatory reduction not only of S0 but also oxidized forms of metals. Intensity of anaerobic respiration of microorganisms in polluted environments is determined by level of their adaptation to stress factors, in particular, copper (II) compounds. The aim of this work was to investigate the influence of copper (II) chloride on H2S production by Desulfuromonas sp. strains isolated by us from Yavorivske Lake, to determine the efficiency of Cu2+ precipitation by hydrogen sulfide, to analyse the possibility of usage by bacteria of CuCl2 as an electron acceptor of anaerobic respiration and to study the influence of Cu2+ on usage by these microorganisms of ferric (III) citrate, potassium dichromate or manganese (IV) oxide as electron acceptors. Bacteria were grown under anaerobic conditions in Kravtsov-Sorokin medium. To study the influence of Cu2+ on production by bacteria of H2S, their cells were incubated with CuCl2 (0.5–4.0 mM), washed and cultivated in a medium with S0. To determine the level of Cu2+ binding by H2S, produced by bacteria, cells were grown in a medium with CuCl2 (0.5–4.0 mM) and S0. To investigate the ability of bacteria to use copper (II) ions as electron acceptors, they were cultivated in a medium with CuCl2 (1.74–10.41 mM). To study the influence of Cu2+ on usage by bacteria of metal compounds as electron acceptors, their cells were incubated with CuCl2 (0.5–4.0 mM), washed and cultivated in media with C6H5O7Fe, K2Cr2O7 or MnO2 (1.74–10.41 mM). Biomass was determined by the turbidimetric method. In the cultural liquid the content of H2S was determined quantitatively by the spectrophotometric method, qualitatively – presence of Cu2+. Content of CuS in the growth medium was determined by weight method. Desulfuromonas sp. bacteria was revealed to be resistant to 2.0–2.5 mM copper (II) ions. Under the influence of 3.0–4.0 mM CuCl2 in the incubation mixture, sulfidogenic activity of bacteria decreased more than twice. The efficiency of Cu2+ binding in form of CuS by H2S produced by bacteria reached 97.3–100.0% at presence in the medium with S0 of up to 1.5 mM CuCl2. Bacteria used CuCl2 (1.74–10.41 mM) as an electron acceptor in the process of anaerobic respiration. The addition of 2.5–3.0 mM CuCl2 to the incubation mixture caused inhibition of metal reducing activity of cells, growth of all strains in media with 1.74–10.41 mM ferric (III) citrate, potassium dichromate or manganese (IV) oxide as electron acceptors decreased by 2.6 times. Almost complete precipitation up to 1.5 mM copper (II) ions in form of CuS by H2S produced by bacteria and ability to reduce up to 10.41 mM CuCl2, C6H5O7Fe, K2Cr2O7 or MnO2 in the process of anaerobic respiration indicates a high adaptation of the bacteria strains investigated by us to stress factors, in particular, the influence of CuCl2. We have proved the possibility of using Desulfuromonas sp. in biotechnologies for purification of environments with complex contamination from copper (II) compounds.

References

Behlau, F., Gochez, A. M., Lugo, A. J., Elibox, W., Minsavage, G. V., Potnis, N., White, F. F., Ebrahim, M., Jones, J. B., & Ramsubhag, A. (2017). Characterization of a unique copper resistance gene cluster in Xanthomonas campestris pv. campestris isolated in Trinidad, West Indies. European Journal of Plant Pathology, 147(3), 671–681.


Betehtin, A. G. (2007). Kurs mineralogii [The course of mineralogy]. KDU, Moscow (in Russian).


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.


Breuer, M., Rosso, K. M., Blumberger, J., & Butt, J. N. (2015). Multi-haem cytochromes in Shewanella oneidensis MR-1: Structures, functions and opportunities. Journal of the Royal Society Interface, 12(102), 20141117.


Cidre, I., Pulido, R. P., Grande Burgos, M. J., Gálvez, A., & Lucas, R. (2017). Copper and zinc tolerance in bacteria isolated from fresh produce. Journal of Food Protection, 80(6), 969–975.


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.


Diakiv, S. V., Hnatush, S. O., Babenko, V. V., & Moroz, O. M. (2017). Sul'fidogenna aktyvnist' Desulfuromusa sp. SV30 za vplyvu spoluk hromu, kuprumu i ferumu [Sulfidogenic activity of Desulfuromusa sp. SV30 under the influence of chromium, copper and iron compounds]. Studia Biologica, 11(2), 53–66 (in Ukrainian).


Diakiv, S. V., Hnatush, S. O., Moroz, O. M., Prypin, O. Y., Kulachkovskyi, O. R., & Bodnaruk, V. Y. (2016). Sulfur reducing bacteria from coal pits waste heaps of Chervonograd Mining Region. Studia Biologica, 10(2), 63–76.


Frank, Y. A., & Lushnikov, S. V. (2006). Biotekhnologicheskij potencial sul'fatreduciruyushchih bakterіj [Biotechnological potential of sulfate reducing bacteria]. Ehkologiya i Promyshlennost', 1, 10–13 (in Russian).


Gescher, J., & Kappler, A. (2012). Microbial metal respiration: From geochemistry to potential applications. Springer-Verlag, Heidelberg, Berlin.


Gillan, D. C., van Camp, C., Mergeay, M., Provoost, A., Thomas, N., Vermard, L., Billon, G., & Wattiez, R. (2017). Paleomicrobiology to investigate copper resistance in bacteria: Isolation and description of Cupriavidus necator B9 in the soil of a medieval foundry. Environmental Microbiology, 19(2), 770–787.


Gochez, A. M., Huguet-Tapia, J. C., Minsavage, G. V., Shantaraj, D., Jalan, N., Strauß, A., Lahaye, T., Wang, N., Canteros, B. I., Jones, J. B., & Potnis, N. (2018). PacBio sequencing of copper-tolerant Xanthomonas citri reveals presence of a chimeric plasmid structure and provides insights into reassortment and shuffling of transcription activator-like effectors among X. citri strains. BMC Genomics, 19(16), 1–14.


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]. Mikrobiologichny 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 B-7384 [Certificate of deposition of bacteria Desulfuromonas acetoxidans Ya-2006 strain at the Depository of D. K. Zabolotny Institute of Microbiology and Virology of the NAS of Ukraine with appropriation of registration number IMV B-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]. Ivan Franko National University of L’viv, Lviv (in Ukrainian).


Harris, D. S. (2003). Quantitative chemical analysis. Amazon, New York.


Hedderich, R., Klimmek, O., Kroger, A., Dirmeier, R., Keller, M., & Stetter, K. O. (1999). Anaerobic respiration with elemental sulfur and with disulfides. FEMS Microbiology Reviews, 22(5), 353–381.


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. Journal of Bioscience and Bioengineering, 117(3), 333–335.


Kiran, M. G., Pakshirajan, K., & Das, G. (2017). Heavy metal removal from multicomponent system by sulfate reducing bacteria: Mechanism and cell surface characterization. Journal of Hazardous Materials, 324(A), 62–70.


Kozlova, I. P., Radchenko, O. S., Stepura, L. H., Kondratyuk, T. O., & Pilyashenko-Novokhatnyy, A. I. (2008). Heokhimichna diyalnist mikroorhanizmiv ta yiyi prykladni aspekty [Geochemical activity of microorganisms and its applied aspects]. Naukova Dumka, Kyiv (in Ukrainian).


Kucherjavyj, V. P. (2001). Ekologija [Ecology]. Svit, Lviv (in Ukrainian).


Kumar, A., Bisht, B. S., & Joshi, V. D. (2010). Biosorption of heavy metals by four acclimated species, Bacillus spp., Pseudomonas spp., Staphylococcus spp. and Aspergillus niger. Journal of Biological and Environmental Sciences, 4(12), 97–108.


Kuznetsov, A., Gradova, N., Lushnikov, S., Éngelkhart, M., Vaysser, T., & Chebotareva, M. (2015). Prikladnaya ehkobiotekhnologiya [Applied Ecobiotechnology]. Binom Laboratoriya Znanij, Moscow (in Russian).


Ladomersky, E., & Petris, M. J. (2015). Copper tolerance and virulence in bacteria. Metallomics, 7, 957–964.


Lengeler, J., Drevs, G., & Shlegel, G. (Eds.). (2005). Sovremennaya mikrobiologiya. Prokarioty [Contemporary 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. Ecotoxicology and Environmental Safety, 122, 322–330.


Martínez-Bussenius, C., Navarro, C. A., & Jerez, C. A. (2017). Microbial copper resistance: Importance in biohydrometallurgy. Microbial Biotechnology, 10(2), 279–295.


Maslovska, O., & Hnatush, S. (2015). Oxidative modification of proteins and specific superoxide dismuase activity of Desulfuromonas acetoxidans ІМV В-7384 bacteria under the influence of ferric citrate. Microbiology and Biotechnology, 30, 34–40.


Moroz, O. M. (2013). Utvorennya hidrohen sulʹfidu sirkovidnovlyuvalʹnymy bakteriyamy za vplyvu soley vazhkykh metaliv [Hydrogen sulfide production by sulfur reducing bacteria under the influence of heavy metal salts]. Visnyk of L’viv University. Biological Series, 61, 154–165 (in Ukrainian).


Moroz, O. M., Hnatush, S. O., Bohoslavets, C. I., Yavorska, G. V., Zvir, G. I., & Borsukevych, B. M. (2017). Vplyv kalij bihromatu na dejaki fiziologichni osoblyvosti bakterij cyklu sul'furu ozera Javorivs'ke [Potassium dichromate influence on some physiological peculiarities of sulfur cycle bacteria from Yavorivske lake]. Visnyk of L’viv University. Biological Series, 75, 127–139 (in Ukrainian).


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]. Visnyk of L’viv University. Biological Series, 65, 322–334 (in Ukrainian).


Mustapha, M. U., & Halimoon, N. (2015). Screening and isolation of heavy metal tolerant bacteria in industrial effluent. Procedia Environmental Sciences, 30, 33–37.


Richard, D., Boyer, C., Vernière, C., Canteros, B. I., Lefeuvre, P., & Pruvost, O. (2017a). Complete genome sequences of six copper-resistant Xanthomonas citri pv. citri strains causing Asiatic citrus canker, obtained using long-read technology. Genome Announcements, 5(12), e00010-17.


Richard, D., Ravigné, V., Rieux, A., Facon, B., Boyer, C., Boyer, K., Grygiel, P., Javegny, S., Terville, M., Canteros, B. I., Robène, I., Vernière, C., Chabirand, A., Pruvost, O., & Lefeuvre, P. (2017b). Adaptation of genetically monomorphic bacteria: Evolution of copper resistance through multiple horizontal gene transfers of complex and versatile mobile genetic elements. Molecular Ecology, 26(7), 2131–2149.


Richter, K., Schicklberger, M., & Gescher, J. (2012). Dissimilatory reduction of extracellular electron acceptors in anaerobic respiration. Applied Environmental Microbiology, 78(4), 913–921.


Sani, R. K., Peyton, B. M., & Brown, L. T. (2001). Copper-induced inhibition of growth of Desulfovibrio desulfuricans G20: Assessment of its toxicity and correlation with those of zinc and lead. Applied and Environmental Microbiology, 67(10), 4765–4772.


Segin, T., Hnatush, S., & Gorishniy, M. (2016). Protsesy lipoperoksydatsiyi u klitynakh Chlorobium limicola IMV K-8 za vplyvu Cu (II) sulʹfatu [Lipoperoxidation processes in Chlorobium limicola IMV K-8 cells under the influence of Cu (II) sulfate]. Visnyk of Dnipropetrovsk University. Biology, Ecology, 24(1), 72–78 (in Ukrainian).


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.


Silver, S., & Walderhaug, M. (1995). Bacterial plasmid-mediated resistances to mercury, cadmium and copper. Toxicology of metals. Biochemical aspects. Springer, Berlin.


Simonte, F., Sturm, G., Gescher, J., & Sturm-Richter, K. (2017). Extracellular electron transfer and biosensors. Advances in Biochemical Engineering / Biotechnology. Springer, Berlin, Heidelberg.


Solioz, M., & Stoyanov, J. (2003). Copper homeostasis in Enterococcus hirae. FEMS Microbiology Reviews, 27(2–3), 183–195.


Tashirev, A. B. (1995). Vzaimodejstvie mikroorganizmov s metallami [Interaction of microorganisms with metals]. Mikrobiologicheskij Zhurnal, 57(2), 95–104 (in Russian).


Tashirev, A. B., Galinker, J. V., & Andrejuk, E. I. (2008). Termodinamicheskoe prognozirovanie redoks-vzaimodejstvija mikroorganizmov s metallami-okisliteljami (Hg2+, CrO42– i Cu2+) [Thermodynamic calculations of redox interaction of microorganisms with oxidative metals (Hg2+, CrO42– and Cu2+)]. Doklady NAN Ukrainy, 4, 166–172 (in Russian).


Tashirev, A. B., Matveeva, N. A., Romanovskaja, V. A., Tashireva, A. A., & Rokitko, P. V. (2007). Polirezistentnost' i sverhustojchivost' k tjazhjolym metallam antarkticheskih mikroorganizmov [Polyresistance and superstability of Antarctic microorganisms to heavy metals]. Doklady NAN Ukrainy, 11, 170–175 (in Russian).


Vandieken, V., Mussmann, M., Niemann, H., & Jørgensen, B. B. (2006). Desulfuromonas svalbardensis sp. nov. and Desulfuromusa ferrireducens sp. nov., psychrophilic, Fe(III)-reducing bacteria isolated from arctic sediments, Svalbard. International Journal of Systematic and Evolutionary Microbiology, 56, 1133–1139.


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


White, C., Sayer, J. A., & Gadd, G. M. (2000). Microbial solubilization and immobilization of toxic metals: Key biogeochemical processes for treatment of contamination. FEMS Microbiology Ecology, 33, 197–208.


Winkelmann, G. (Ed.). (2008). Microbial transport systems. Wiley-VCH, New York.

Published
2018-08-20
Section
Articles