The usage of nitrogen compounds by purple non-sulfur bacteria of the Rhodopseudomonas genus

Keywords: phototropic bacteria; nitrite ions; nitrate ions; nitrogen cycle.

Abstract

In this article, we characterized the regularities of oxidation of nitrite ions by phototropic purple non-sulfur bacteria Rhodopseudomonas yavorovii IMV B-7620, which were isolated from the water of Yavorivske Lake (Lviv Region, Ukraine). The bacteria were cultivated anaerobically at the light intensity of 200 lux and aerobically without illumination for 13 days in the modified ATCC No. 1449 medium. The concentration of nitrite ions was determined turbidimetrically by the turbidity of the solution by method of diazotization of sulfanilic acid by the nitrite ions and the interaction of the formed salt with n-(l-naphtyl)ethylenediamine dihydrochloride. The concentration of nitrate ions was determined turbidimetrically by the turbidity of the solution by method of diazotization. Zinc powder was used as a reducing agent. Efficiency of oxidation of 0.7–5.6 mM nitrite ions as electron donors by these bacteria was 100–7%, on the 10-th day of cultivation. It was established that nitrate ions were accumulated in the medium as a result of oxidation of nitrite ions by bacteria. The largest biomass (1.6 g/L) bacteria accumulated on the thirteenth day of growth in a medium with 2.8 mM NO2–. We found that R. yavorovii can use nitrate ions and urea as the only source of nitrogen for phototrophic growth. At a concentration of 1.9 mM ammonium chloride, sodium nitrite and urea in the cultivation medium, the biomass of bacteria was 1.2, 0.8, 1.0 g/L, respectively. The ability of the studied microorganisms to oxidize nitrite ions and to use nitrate ions indicates the significant impact of purple non-sulfur bacteria on the redistribution of streams of nitrogen compounds in ecosystems and the essential role of these microorganisms in the nitrogen biogeochemical cycle.

References

Arashida, H., Kugenuma, T., Watanabe, M., & Maeda, I. (2018). Nitrogen fixati on in Rhodopseudomonas palustris co-cultured with Bacillus subtilis in the presence of air. Journal of Bioscience and Bioengineering, 18, 1389–1723.

Bock, E., Koops, H.-P., Ahlers, B., & Harms, H. (1991). Oxidation of inorganic nitrogen compounds as energy source. In: Balows, A., Trüper, H. G., Dworkin, M., Harder, W., Schleifer, K. H. (Eds.). The prokaryotes. Springer Verlag, New York. Pp. 414–430.

Canfield, D. E., Glazer, A. N., & Falkowski, P. G. (2010). The evolution and future of Earth’s nitrogen cycle. Science, 330, 192–196.

Cusanovich, M. A., Bartsch, R. G., & Kamen, M. D. (1968). Light-induced elect ron transport in Chromatium strain D. II. Light-induced absorbance changes in Chromatium chromatophores. Biochimica et Biophysica Acta – Bioener getics, 153(2), 397–417.

Elser, J. J., Bracken, M. E., Cleland, E. E., Gruner, D. S., Harpole, W. D., Hillebrand, H., Ngai, J. G., Seabloom, E. W., Shurin, J. B., & Smith, J. E. (2007). Global analysis of nitrogen and phosphorus limitation of primary producers in fresh water, marine and terrestrial ecosystems. Ecology Letters, 10(12), 1135–1142.

Galloway, J. N. (1998). The global nitrogen cycle: Changes and consequences. Environmental Pollutions, 102, 15–24.

Galloway, J. N., Leach, A. M., Bleeker, A., & Erisman, J. W. (2013). A chronology of human understanding of the nitrogen cycle. Philosophical Transactions of the Royal Society of London. Series B. Biological Sciences, 368(1621), 20130120.

Ghosh, W., & Dam, B. (2009). Biochemistry and molecular biology of lithotro phic sulfur oxidation by taxonomically and ecologically diverse bacteria and archaea. FEMS Microbiology Reviews, 33(6), 999–1043.

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.

Hallenbeck, P. C. (2017). Modern topics in the phototrophic prokaryotes. Springer International Publishing AG.

Hoffman, B. M., Lukoyanov, D., Yang, Z. Y., Dean, D. R., & Seefeldt, L. C. (2014). Mechanism of nitrogen fixation by nitrogenase: The next stage. Chemical Reviews, 114(8), 4041–4062.

Imhoff, J. F., Hiraishi, A., & Suling, J. (2005). Bergey's manual of systematic bac teriology. The Proteobacteria. Part C. The Alpha-, Beta-, Delta-, and Epsilon proteobacteria. Garrity, G. M, Staley, J. T., Krieg, N. R., & Brenner, D. J. (Eds.). Springer, USA.

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).

Kroneck, P. M. H., & Abt, D. J. (2002). Molybdenum in nitrate reductase and nitrite oxidoreductase. In: Sigel, A., & Sigel, H. (Eds.). Molybdenum and tungsten. Their roles in biological processes. M. Dekker Inc., New York.

Kumar, B. V., Ramprasad, E. V. V., Sasikala, C., & Ramana, C. V. (2013). Rhodo pseudomonas pentothenatexigenes sp. nov. and Rhodopseudomonas thermoto lerans sp. nov., isolated from paddy soils. International Journal of Systematic and Evolutionary Microbiology, 63, 200–207.

Langley, J. A., & Megonigal, J. P. (2010). Ecosystem response to elevated CO2 levels limited by nitrogen-induced plant species shift. Nature, 466, 96–99.

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

Luo, Y., Su, B., Currie, W. S., Dukes, J. S., Finzi, A., Hartwig, U., Hungate, B., Mcmurtrie, R. E., Oren, R., Parton, W. J., Pataki, D. E., Shaw, M. R., Zak, D. R., & Field, C. B. (2004). Progressive nitrogen limitation of ecosystem responses to rising atmospheric carbon dioxide. Bioscience, 54(8), 731–739.

Mackenzie, F. T. (1998). Our changing planet: An introduction to earth system science and global environmental change. Prentice-Hall, Upper Saddle River, New Jersey.

Megonigal, J. P., Hines, M. E., & Visscher, P. T. (2003). Anaerobic metabolism: Linkages to trace gases and aerobic processes. In: Schlesinger, W. H. (Ed.). Treatiseon geochmistry. Elsevier, Amsterdam, 8, 317–424.

Neutzling, O., Imhoff, J. F., & Truper, H. G. (1984). Rhodopseudomonas adriatica sp. nov., a new species of the Rhodospirillaceae, dependent on reduced sulfur compounds. Archives of Microbiology, 137, 256–261.

Olmo-Mira, M. F., Cabello, P., Pino, C., Martınez-Luque, M., Richardson, D. J., Castillo, F., Roldan, M. D., & Moreno-Vivian, C. (2006). Expression and characterization of the assimilatory NADH nitrite reductase from the photo trophic bacterium Rhodobacter capsulatus E1F1. Archives of Microbiology, 186, 339–344.

Ramana, V. V., Chakravarthy, S. K., Raj, P. S., Kumar, B. V., Shobha, E., Rama prasad, E. V. V., Sasikala, C., & Ramana, C. V. (2012). Descriptions of Rho dopseudomonas parapalustris sp. nov., Rhodopseudomonas harwoodiae sp. nov. and Rhodopseudomonas pseudopalustris sp. nov., and emended descrip tion of Rhodopseudomonas palustris. International Journal of Systematic Evolutionary Microbiology, 62, 1790–1798.

Schott, J., Griffin, B. M., & Schink, B. (2010). Anaerobic phototrophic nitrite oxidation by Thiocapsa sp. strain KS1 and Rhodopseudomonas sp. strain LQ17. Microbiology, 156, 2428–2437.

Schwartz, G., Mendel, R. R., & Ribbe, M. W. (2009). Molybdenum cofactors, enzymes and pathways. Nature, 460(7257), 839–847.

Simon, J., & Klotz, M. G. (2013). Diversity and evolution of bioenergetic systems involved in microbial nitrogen compound transformations. Biochimica et Biophysica Acta, 1827, 114–135.

Stein, L. Y., & Klotz, M. G. (2016). The nitrogen cycle. Current Biology, 26(3), R94–R98.

Stolz, J. F., & Basu, P. (2002). Evolution of nitrate reductase: Molecular and structural variations on a common function. ChemBioChem, 3(2–3), 198–206.

Tarabas, O. V., Hnatush, S. O., Moroz, O. M., & Ostash, B. O. (2017b). Svidot stvo pro deponuvannya shtamu bakteriy Rhodopseudomonas yavorovii Ya-2016 z nadannyam reyestracijnogo nomeru IMV B-7620 vid 01.08.2017 u Depozytariyi Instytutu mikrobiolohiyi i virusolohiyi im. D. K. Zabolotnoho NAN Ukrayiny, Kyiv [Certificate of deposition of bacteria Rhodopseudomo nas yavorovii Ya-2016 strain with appropriation of registration number IMV B-7620 from 01.08.2017 at the Depository of D. K. Zabolotny Institute of Microbiology and Virology of the NAS of Ukraine, Kyiv] (in Ukrainian).

Tarabas, O. V., Hnatush, S. O., Moroz, O. M., Vasilechko, V. O., Grishhuk, G. V., Zvіr, G. І., & Komplіkevich, S. J. (2017c). Vykorystannja sul'fid- ta tiosul'fat-joniv purpurovymy nesirkovymy bakterijamy Rhodopseudomonas yavorovii Ya-2016 [The usage of sulfide and thiosulfate ions by purple non-sulfur bacteria Rhodopseudomonas yavorovii Ya-2016]. Biosystems Diver sity, 25(3), 181–185.

Tarabas, O. V., Hnatush, S. O., Ostash, B. O., Mutenko, G. V., & Koshla, O. V. (2017d). Іdentifіkacіja purpurovih nesіrkovih bakterіj Rhodopseudomonas sp. Ya-2016 [Identification of purple non-sulfur bacteria of Rhodopseudomo nas sp. Ya-2016]. Visnyk of Lviv University, Biological Series, 75, 140–145 (in Ukrainian).

Tarabas, O., Hnatush, S., Govorukha, V., Tashyrev, O., & Moroz, О. (2017a). Production of molecular hydrogen by purple non-sulfur bacteria Rhodopseudo monas yavorovii Ya-2016. 7th International Weigl Conference, Lviv. Pp. 188.

Zhang, D., Yang, H., Huang, Z., Zhang, W., & Liu, S. J. (2002). Rhodopseudo monas faecalis sp. nov., a phototrophic bacterium isolated from an anaerobic reactor that digests chicken faeces. International Journal of Systematic Evolutionary Microbiology, 52, 2055–2060.

Published
2019-02-16
How to Cite
TarabasО. V., HnatushS. О., & МorozО. М. (2019). The usage of nitrogen compounds by purple non-sulfur bacteria of the Rhodopseudomonas genus . Regulatory Mechanisms in Biosystems, 10(1), 83-86. https://doi.org/10.15421/021913