Influence of potassium dichromate on the reduction of sulfur, nitrate and nitrite ions by bacteria Desulfuromonas sp.

  • O. M. Moroz Ivan Franko National University
  • S. O. Hnatush Ivan Franko National University of Lviv
  • H. V. Yavorska Ivan Franko National University of Lviv
  • G. I. Zvir Ivan Franko National University of Lviv
  • O. V. Tarabas Ivan Franko National University of Lviv
Keywords: Desulfuromonas sp.; sulfur; nitrate ions; nitrite ions; hexavalent chromium; electron acceptors

Abstract

This article presents the regularities of reduction of sulfur, nitrate and nitrite ions by sulfur reducing bacteria Desulfuromonas sp., which were isolated from the water of the man-made Yavorivske Lake (Lviv Region, Ukraine), under the influence of potassium dichromate. This bacteria in the process of anaerobic respiration can use and reduce different electron acceptors, such as sulfur, nitrates, nitrites, oxidized forms of heavy metals, in particular, hexavalent chromium. Technogenically altered ecotopes are characterized by complex pollution, so several electron acceptors are available to bacteria at the same time. Strains of microorganisms isolated from such ecotopes are adapted to unfavourable conditions and therefore have high biotechnological potential. The purpose of this work was to investigate the regularities of elemental sulfur, nitrate or nitrite ion usage by sulfidogenic bacteria of Desulfuromonas genus in conditions of simultaneous presence in the medium of another electron acceptor – Cr(VI), to establish the succession of reduction of electron acceptors by strains of these bacteria and to evaluate the efficiency of their possible application in technologies of complex purification of the environment from metal compounds and other inorganic toxicants. Bacteria were grown under anaerobic conditions in Kravtsov-Sorokin medium without SO42– and without Mohr’s salt for 10 days. To study the efficiency of sulfur, nitrate or nitrite ions’ reduction at simultaneous presence in the medium of Cr(VI) bacteria were sown in media with elemental sulfur, NaNO3, NaNO2 or K2Cr2O7 to final S0, NO3–, NO2–or Cr(VI) concentration in the medium of 3.47 (concentration of SO42– in medium of standard composition) or 1.74, 3.47, 5.21, 6.94 and 10.41 mM. Biomass was determined by the turbidimetric method, and the concentrations of nitrate, nitrite, ammonium ions, hydrogen sulfide, Cr(VI), Cr(ІІІ) in cultural liquid were determined spectrophotometrically. It has been established that Cr(VI) inhibits the biomass accumulation and hydrogen sulfide production by bacteria of Desulfuromonas sp. after simultaneous addition into the medium of 3.47 mM S0 and 1.74–10.41 mM Cr(VI). In the medium with the same initial content (3.47 mM) of S0 and Cr(VI) bacteria produced Cr(III) at concentrations 3.3–3.4 times higher than that of hydrogen sulfide. It has been shown that K2Cr2O7 inhibits biomass accumulation, nitrate ions’ reduction and ammonium ions’ production by bacteria after simultaneous addition into the medium of 3.47 mM NO3– and 1.74–10.41 mM Cr(VI) or 1.74–10.41 mM NO3– and 3.47 mM Cr(VI). In the medium with the same initial content (3.47 mM) of NO3– and Cr(VI) bacteria reduced up to 1.2 times more nitrate ions than Cr(VI) with the production of ammonium ions at concentrations the same times higher than those of Cr(III). It has been established that K2Cr2O7 inhibits biomass accumulation, nitrite ions’ reduction and ammonium ions’ production by bacteria after simultaneous addition into the medium of 3.47 mM NO2– and 1.74–10.41 mM Cr(VI) or 1.74–10.41 mM NO2– and 3.47 mM Cr(VI). In the medium with the same initial content of (3.47 mM) NO2– and Cr(VI) the reduction of Cr(VI) by bacteria was only slightly, up to 1.1 times, lower than the reduction of nitrite ions, almost the same concentrations of trivalent chromium and ammonium ions were detected in the cultural liquid. The processes of nitrate and nitride reduction carried out by bacteria of Desulfuromonas genus were revealed to be less sensitive to the negative influence of sodium dichromate, as compared with the process of sulfur reduction, because in the media with the same initial content (3.47 mM) of NO3– or NO2– and Cr(VI) bacteria produced 1.1–1.2 times more NH4+ than Cr(III), but in the medium with the same initial content (3.47 mM) of S0 and Cr(VI) ) bacteria produced over than three times more Cr(III) than hydrogen sulfide. Our data allow us to conclude that bacteria of Desulfuromonas genus, the investigated strains of which are adapted to high concentrations (up to 10.41 mM) of inorganic toxicants, play an important role in the geochemical cycles of sulfur, nitrogen and chromium in aquatic environments that have been under anthropogenic influence.

References

Aguilar-Barajas, E., Diaz-Perez, C., Ramirez-Diaz, M. I., Riveros-Rosas, H., & Cervantes, C. (2011). Bacterial transport of sulfate, molybdate, and related oxyanions. Biometals, 24, 687–707.

An, T. T., & Picarda, F. W. (2015). Desulfuromonas carbonis sp. nov., an Fe (III)-, S0 and Mn (IV)-reducing bacterium isolated from an active coalbed methane gas well. International Journal of Systematic and Evolutionary Microbiology, 65(5), 1686–1693.

Belchik, S. M., Kennedy, D. W., Dohnalkova, A. C., Wang, Y. M., Sevinc, P. C., Wu, H., Lin, Y. H., Lu, H. P., Fredrickson, J. K., & Shi, L. (2011). Extracellular reduction of hexavalent chromium by cytochromes MtrC and OmcA of Shewanella oneidensis MR-1. Applied and Environmental Microbiology, 77(12), 4035–4041.

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.

Bokranz, M. J., Katz, J., Schröder, I., Roberton, A. M., & Kröger, A. (1983). Energy metabolism and biosynthesis of Vibrio succinogenes growing with nitrate or nitrite as terminal electron acceptor. Archives of Microbiology, 135, 36–41.

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.

Caballero-Flores, G. G., Costa-Navarrete, Y. M., Ramirez-Diaz, M. I., Silva-Sanchez, J., & Cervantes, C. (2012). Chromate-resistance genes in plasmids from antibiotic-resistant nosocomial enterobacterial isolates. FEMS Microbiology Letters, 327(2), 148–154.

Cadby, I. T., Faulkner, M., Cheneby, J., Long, J., van Helden, J., Dolla, A., & Cole, J. A. (2017). Coordinated response of the Desulfovibrio desulfuricans 27774 transcriptome to nitrate, nitrite and nitric oxide. Scientific Reports, 7, 16228.

Chayka, O. M., & Peretyatko, T. B. (2018). The reduction of hexavalent chromium and nitrates by Desulfuromonas sp. YSDS-3, isolated from the soil of Yasiv sulfur mine. Ecology and Noospherology, 29(2), 76–82.

Chayka, O., Peretyatko, T., Gudz, S., & Hnatush, S. (2016). Sulfur reducing activity of the Desulfuromonas acetoxidans IMV B-7384 under different cultivation conditions. Visnyk of Lviv University, Biological Series, 74, 161–168.

Fathima, N. N., Aravindhan, R., Rao, J. R., & Nair, B. U. (2005). Solid waste removes toxic liquid waste: Adsorption of chromium (VI) by iron complexed protein waste. Environmental Science and Technology, 39(8), 2804–2810.

Fitzgerald, L. A., Petersen, E. R., Leary, D. H., Nadeau, L. J., Soto, C. M., Ray, R. I., Little, B. J., Ringeisen, B. R., Johnson, G. R., Vora, G. J., & Biffinger, J. C. (2013). Shewanella frigidimarina microbial fuel cells and the influence of divalent cations on current output. Biosensors and Bioelectronics, 40(1), 102–109.

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

Govorukha, V. M., Havrylyuk, O. A., & Tashyrev, O. B. (2015). Regularities of quantitative distribution for Fe(III)-reducing bacteria in natural ecosystems. Biotechnologia Acta, 8(3), 123–128.

Granger, D. L., Taintor, R. R., Boockvar, K. S., & Hibbs, J. B. (1996). Measurement of nitrate and nitrite in biological samples using nitrate reductase and Griess reaction. Methods Enzymology, 268, 142–151.

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 Lviv, Lviv (in Ukrainian).

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.

Hnatush, S. O., Moroz, O. M., Yavorska, G. V., & Borsukevych, B. M. (2018). Sulfidogenic and metal reducing activities of Desulfuromonas genus bacteria under the influence of copper chloride. Biosystems Diversity, 26(3), 218–226.

Hnatush, S., & Maslovska, O. (2018). Sulfur-reducing bacteria Desulfuromonas acetoxidans ІМV В-7384 under the influence of heavy metal ions. The Development of Natural Sciences. Baltija Publishing, Riga.

Hoffmann, M. C., Pfänder, Y., Tintel, M., & Masepohl, B. (2017). Bacterial PerO permeases transport sulfate and related oxyanions. Journal of Bacteriology, 199(14), e00183-17.

Jing, X., Wu, Y., Shi, L., Peacock, C. L., Ashry, N. M., Gao, C., Huang, Q., & Cai, P. (2020). Outer membrane c-type cytochromes OmcA and MtrC play distinct roles in enhancing the attachment of Shewanella oneidensis MR-1 cells to goethite. Applied and Environmental Microbiology, 86(23), e01941-20.

Joutey, N. T., Sayel, H., Bahafid, W., & El Ghachtouli, N. (2015). Mechanisms of hexavalent chromium resistance and removal by microorganisms. Reviews of Environmental Contamination and Toxicology, 233, 45–69.

Kazakis, N., Kougias, I., & Patsialis, T. (2015). Assessment of flood hazard areas at a regional scale using an index-based approach and analytical hierarchy process: Application in Rhodope-Evros Region, Greece. Science of the Total Environment, 538, 555–563.

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).

Kuever, J., Rainey, F. A., & Widdel, F. (2005). Family I. Desulfuromonaceae fam. nov. Genus I. Desulfuromonas / Desulfuromonas genus. Pfennig and Biebl, 1977. In: Brenner, D. J., Krieg, N. R., Staley, J. T., & Garrity, G. M. (Eds.). Bergey’s manual of systematic bacteriology. Vol. 2. Springer, New York.

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

Lengeler, J., Drevs, G., & Shlegel, G. (Eds.). (2005). Sovremennaya mikrobiologiya. Prokarioty [Contemporary Microbiology. Prokaryotes]. Mir, Moscow (in Russian).

Liang, J., Huang, X., Yan, J., Li, Y., Zhao, Z., Liu, Y., Ye, J., & Wei, Y. (2021). A review of the formation of Cr(VI) via Cr(III) oxidation in soils and groundwater. Science of the Total Environment, 774, 145762.

Mandich, N. V. (1997). Chemistry and theory of chromium deposition: Part I – Chemistry. Plating and Surface Finishing, 84(5), 108–115.

Maslovska, O. D., & Hnatush, S. O. (2013). Vplyv ferum (III) cytratu na ATF-gidrolazy Desulfuromonas acetoxidans IMV B-7384 [The influence of ferric (III) citrate on ATP-hydrolases of Desulfuromonas acetoxidans ІМV В-7384]. Biosystems Diversity, 21(1), 3–8 (in Ukrainian).

Maslovska, O., Hnatush, S., & Katernyak, S. (2015). The activity of enzymes of glutathione antioxidant system of Desulfuromonas acetoxidans ІМV B-7384 under the influence of ferric (III) citrate. Visnyk of Lviv University, Biological Series, 70, 213–220.

McKinlay, J. B., Cook, G. M., & Hards, K. (2020). Microbial energy management – a product of three broad tradeoffs. Advances in Microbial Physiology, 77, 139–185.

Moroz, O. M., Hnatush, S. O., Bohoslavets, C. I., Yavorska, G. V., & Truchym, N. V. (2016). Vykorystannya bakteriyamy Desulfuromonas sp. yoniv ferumu (III) i manhanu (IV) yak aktseptoriv elektroniv [Usage of ferrum (ІІІ) and manganese (IV) ions as electron acceptors by bacteria of Desulfuromonas sp.]. Biosystems Diversity, 24(1), 87–95 (in Ukrainian).

Moroz, O. M., Hnatush, S. O., Tarabas, O. V., Bohoslavets, C. I., Yavorska, G. V., & Borsukevych, B. M. (2018). Sulfidogenna aktyvnist sulfatvidnovlyuvalnyh i sirkovidnovlyuvalnyh bakteriy za vplyvu spoluk metaliv [Sulfidogenic activity of sulfate and sulfur reducing bacteria under the influence of metal compounds]. Biosystems Diversity, 26(1), 3–10 (in Ukrainian).

Moroz, O. M., Peretyatko, T. B., Klym, I. R., Borsukevych, B. M., Yavorska, G. V., & Kulachkovsky, O. R. (2013). Sirkovidnovlyuvalni bakteriyi ozera Yavorivske: Deyaki morfolohichni, kulturalni i fiziolohichni osoblyvosti [Sulfur reducing bacteria from Yavorivske lake: Some morphological, cultural and physiological peculiarities]. Scientific Bulletin of the Uzhgorod University, Series Biology, 35, 34–41 (in Ukrainian).

Moroz, O., Gul, N., Galushka, A., Zvir, G., & Borsukevych, B. (2014). Vykorystannya riznyh akceptoriv elektroniv bakteriyamy Desulfuromonas sp., vydilenymy z ozera Yavorivske [Different electron acceptors usage by bacteria of Desulfuromonas sp. isolated from Yavorivske Lake]. Visnyk of Lviv University, Biological Series, 65, 322–334 (in Ukrainian).

Morozkina, E. V., & Zvyagilskaya, R. A. (2007). Nitrate reductases: Structure, functions, and effect of stress factors. Biochemistry, 72(10), 1151–1160.

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

Poopal, A. C., & Laxman, R. S. (2009). Studies on biological reduction of chromate by Streptomyces griseus. Journal of Hazardous Materials, 169, 539–545.

Prokhorova, A., Sturm-Richter, K., Doetsch, A., & Gescher, J. (2017). Resilience, dynamics and interactions within a multi-species exoelectrogenic model biofilm community. Applied Environmental Microbiology, 83(6), e03033–e03016.

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

Roden, E. E., & Lovley, D. R. (1993). Dissimilatory Fe (III) reduction by the marine microorganism Desulfuromonas acetoxidans. Applied Environmental Microbiology, 59(3), 734–742.

Rosenberg, E., DeLong, E. F., Lory, S., Stackebrandt, E., & Thompson, F. (Eds.). (2014). The Procaryotes. Prokaryotic Physiology and Biochemistry. Springer-Verlag, Berlin, Heidelberg.

Sharma, P., Singh, S. P., Parakh, S. K., & Tong, Y. W. (2022). Health hazards of hexavalent chromium (Cr (VI)) and its microbial reduction. Bioengineered, 13(3), 4923–4938.

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

Sobol, Z., & Schiestl, R. H. (2012). Intracellular and extracellular factors influencing Cr(VI) and Cr(III) genotoxicity. Environmental and Molecular Mutagenesis, 53, 94–100.

Sung, Y., Ritalahti, K. M., Sanford, R. A., Urbance, J. W., Flynn, S. J., Tiedje, J. M., & Löffler, F. E. (2003). Characterization of two tetrachloroethene-reducing, acetate-oxidizing anaerobic bacteria and their description as Desulfuromonas michiganensis sp. nov. Applied Environmental Microbiology, 69(5), 2964–2974.

Teng, Y., Xu, Y., Wang, X., & Christie, P. (2019). Function of biohydrogen metabolism and related microbial communities in environmental bioremediation. Frontiers in Microbiology, 10, 106.

Vasyliv, O. M., Maslovska, О. D., Hnatush, S. O., Bilyy, O. I., & Ferensovych, Y. P. (2016). Electric current generation by Desulfuromonas acetoxidans IMV B-7384 while application of ferric citrate, fuchsine and methylene blue. Microbiology and Biotechnology, 4(36), 42–49.

Vasyliv, O. М., Maslovska, O. D., Ferensovych, Y. P., Bilyу, O. І., & Hnatush, S. O. (2015). Interconnection between tricarboxylic acid cycle and energy generation in microbial fuel cell performed by Desulfuromonas acetoxidans ІМV В-7384. Proceedings of SPIE, 9493, 1–7.

Vasyliv, O., Bilyy, O., Hnatush, S., Kushkevych, I., & Getman, V. (2011). The changes of spectroscopic characteristics of sulfur reducing bacteria Desulfuromonas acetoxidans under the influence of different metal ions. Proceedings of SPIE, 8152, 1–7.

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.

Published
2022-06-04
How to Cite
Moroz, O. M., Hnatush, S. O., Yavorska, H. V., Zvir, G. I., & Tarabas, O. V. (2022). Influence of potassium dichromate on the reduction of sulfur, nitrate and nitrite ions by bacteria Desulfuromonas sp . Regulatory Mechanisms in Biosystems, 13(2), 153-167. https://doi.org/10.15421/022220