1887

Abstract

In anaerobic enrichment cultures for phototrophic nitrite-oxidizing bacteria from different freshwater sites, two different cell types, i.e. non-motile cocci and motile, rod-shaped bacteria, always outnumbered all other bacteria. Most-probable-number (MPN) dilution series with samples from two freshwater sites yielded only low numbers (≤3×10 cm) of phototrophic nitrite oxidizers. Slightly higher numbers (about 10 cm) were found in activated sewage sludge. Anaerobic phototrophic oxidation of nitrite was studied with two different isolates, the phototrophic sulfur bacterium strain KS1 and the purple nonsulfur bacterium strain LQ17, both of which were isolated from activated sludge collected from the municipal sewage treatment plant in Konstanz, Germany. Strain KS1 converted 1 mM nitrite stoichiometrically to nitrate with concomitant formation of cell matter within 2–3 days, whereas strain LQ17 oxidized only up to 60 % of the given nitrite to nitrate within several months with the concomitant formation of cell biomass. Nitrite oxidation to nitrate was strictly light-dependent and required the presence of molybdenum in the medium. Nitrite was oxidized in both the presence and absence of oxygen. Nitrite inhibited growth at concentrations higher than 2 mM. Hydroxylamine and hydrazine were found to be toxic to the phototrophs in the range 5–50 μM and did not stimulate phototrophic growth. Based on morphology, substrate-utilization pattern, absorption spectra, and 16S rRNA gene sequence similarity, strain KS1 was assigned to the genus and strain LQ17 to the genus . Also, strains DSM 217 and DSM 221 were found to oxidize nitrite to nitrate with concomitant growth. We conclude that the ability to use nitrite phototrophically as electron donor is widespread in nature, but low MPN counts indicate that its contribution to nitrite oxidation in the studied habitats is rather limited.

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2010-08-01
2019-08-24
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References

  1. American Public Health Association ( 1965; ). Standard Methods for the Examination of Water and Wastewater Including Bottom Sediments and Sludge, pp. 604–609. New York: American Public Health Association.
  2. Asao, M., Takaichi, S. & Madigan, M. T. ( 2007; ). Thiocapsa imhoffii, sp. nov., an alkaliphilic purple sulfur bacterium of the family Chromatiaceae from Soap Lake, Washington (USA). Arch Microbiol 188, 665–675.[CrossRef]
    [Google Scholar]
  3. Bock, E., Koops, H.-P., Ahlers, B. & Harms, H. ( 1991; ). Oxidation of inorganic nitrogen compounds as energy source. In The Prokaryotes, 2nd edn, pp. 414–430. Edited by A. Balows, H. G. Trüper, M. Dworkin, W. Harder & K.-H. Schleifer. New York: Springer.
  4. Broda, E. ( 1977; ). Two kinds of lithotrophs missing in nature. Z Allg Mikrobiol 17, 491–493.[CrossRef]
    [Google Scholar]
  5. Bussmann, I., Philipp, B. & Schink, B. ( 2001; ). Factors influencing the cultivability of lake water bacteria. J Microbiol Methods 47, 41 [CrossRef]
    [Google Scholar]
  6. Castillo, F. & Cárdenas, J. ( 1982; ). Nitrate reduction by photosynthetic purple bacteria. Photosynth Res 3, 3–18.[CrossRef]
    [Google Scholar]
  7. Caumette, P., Guyoneaud, R., Imhoff, J. F., Süling, J. & Gorlenko, V. ( 2004; ). Thiocapsa marina sp. nov., a novel, okenone-containing, purple sulfur bacterium isolated from brackish coastal and marine environments. Int J Syst Evol Microbiol 54, 1031–1036.[CrossRef]
    [Google Scholar]
  8. Cline, J. D. ( 1969; ). Spectrophotometric determination of hydrogen sulfide in natural waters. Limnol Oceanogr 14, 454–458.[CrossRef]
    [Google Scholar]
  9. Cusanovich, M. A., Bartsch, R. G. & Kamen, M. D. ( 1968; ). Light-induced electron transport in Chromatium strain D. II. Light-induced absorbance changes in Chromatium chromatophores. Biochim Biophys Acta 153, 397–417.[CrossRef]
    [Google Scholar]
  10. de Wit, R. & van Gemerden, H. ( 1987; ). Chemolithotrophic growth of the phototrophic sulfur bacterium Thiocapsa roseopersicina. FEMS Microbiol Ecol 45, 117–126.
    [Google Scholar]
  11. Dunstan, R. H., Kelley, B. C. & Nicholas, D. J. ( 1982; ). Fixation of dinitrogen derived from denitrification of nitrate in a photosynthetic bacterium, Rhodopseudomonas sphaeroides forma sp. denitrificans. J Bacteriol 150, 100–104.
    [Google Scholar]
  12. Edwards, U., Rogall, T., Blöcker, H., Emde, M. & Böttger, E. C. ( 1989; ). Isolation and direct complete nucleotide determination of entire genes. Characterization of a gene coding for 16S ribosomal RNA. Nucleic Acids Res 17, 7843–7853.[CrossRef]
    [Google Scholar]
  13. Fukuoka, M., Fukumori, Y. & Yamanaka, T. ( 1987; ). Nitrobacter winogradskyi cytochrome a 1 c 1 is an iron–sulfur molybdoenzyme having hemes a and c 1. J Biochem 102, 525–530.
    [Google Scholar]
  14. Gogotov, I. N. & Glinskii, V. P. ( 1973; ). Comparative study of nitrogen fixation in the purple bacteria. Mikrobiologiia 42, 983–986.
    [Google Scholar]
  15. Griffin, B. M., Schott, J. & Schink, B. ( 2007; ). Nitrite, an electron donor for anoxygenic photosynthesis. Science 316, 1870 [CrossRef]
    [Google Scholar]
  16. Henckel, T., Friedrich, M. & Conrad, R. ( 1999; ). Molecular analyses of the methane-oxidizing microbial community in rice field soil by targeting the genes of the 16S rRNA, particulate methane monooxygenase, and methanol dehydrogenase. Appl Environ Microbiol 65, 1980–1990.
    [Google Scholar]
  17. Herbert, R. A. ( 1985; ). Development of mass blooms of photosynthetic bacteria on sheltered beaches in Scapa Flow, Orkney Islands. Proc R Soc Edinburgh 87B, 15–25.
    [Google Scholar]
  18. Herbert, R. A., Ranchou-Peyruse, A., Duran, R., Guyoneaud, R. & Schwabe, S. ( 2005; ). Characterization of purple sulfur bacteria from the South Andros Black Hole cave system: highlights taxonomic problems for ecological studies among the genera Allochromatium and Thiocapsa. Environ Microbiol 7, 1260–1268.[CrossRef]
    [Google Scholar]
  19. Hougardy, A., Tindall, B. J. & Klemme, J.-H. ( 2000; ). Rhodopseudomonas rhenobacensis sp. nov., a new nitrate-reducing purple non-sulfur bacterium. Int J Syst Bacteriol 50, 985–992.[CrossRef]
    [Google Scholar]
  20. Klemme, J. H. ( 1979; ). Occurrence of assimilatory nitrate reduction in phototrophic bacteria of the genera Rhodospirillum and Rhodopseudomonas. Microbiologica 2, 415–420.
    [Google Scholar]
  21. Kondratieva, E. N., Zhukov, V. G., Ivanovsky, R. N., Petrushkova, Y. P. & Monosov, E. Z. ( 1976; ). The capacity of phototrophic sulfur bacterium Thiocapsa roseopersicina for chemosynthesis. Arch Microbiol 108, 287–292.[CrossRef]
    [Google Scholar]
  22. Kroneck, P. M. H. & Abt, D. J. ( 2002; ). Molybdenum in nitrate reductase and nitrite oxidoreductase. In Molybdenum and Tungsten. Their Roles in Biological Processes, pp. 369–403. Edited by A. Sigel & H. Sigel. New York: M. Dekker.
  23. Krüger, B., Meyer, O., Nagel, M., Andreesen, J. R., Meincke, M., Bock, E., Blümle, S. & Zumft, W. G. ( 1987; ). Evidence for the presence of bactopterin in the eubacterial molybdoenzymes nicotinic acid dehydrogenase, nitrite oxidoreductase, and respiratory nitrate reductase. FEMS Microbiol Lett 48, 225–227.[CrossRef]
    [Google Scholar]
  24. Lane, D. J., Pace, B., Olsen, G. J., Stahl, D. A., Sogin, M. L. & Pace, N. R. ( 1985; ). Rapid determination of 16S ribosomal RNA sequences for phylogenetic analyses. Proc Natl Acad Sci U S A 82, 6955–6959.[CrossRef]
    [Google Scholar]
  25. Lee, D. Y., Ramos, A., Macomber, L. & Shapleigh, J. P. ( 2002; ). Taxis response of various denitrifying bacteria to nitrate and nitrite. Appl Environ Microbiol 68, 2140–2147.[CrossRef]
    [Google Scholar]
  26. Ludwig, W., Strunk, O., Westram, R., Richter, L., Meier, H., Yadhukumar, Buchner, A., Lai, T., Steppi, S. & other authors ( 2004; ). arb: a software environment for sequence data. Nucleic Acids Res 32, 1363–1371.[CrossRef]
    [Google Scholar]
  27. Madigan, M. T. & Martinko, J. M. ( 2006; ). Brock Biology of Microorganisms, 11th edn, p. 992. Upper Saddle River, NJ: Pearson Prentice Hall.
  28. Madigan, M., Cox, S. S. & Stegeman, R. A. ( 1984; ). Nitrogen fixation and nitrogenase activities in members of the family Rhodospirillaceae. J Bacteriol 157, 73–78.
    [Google Scholar]
  29. Malofeeva, I. V. & Laush, D. ( 1976; ). Utilization of nitrogen compounds by phototrophic bacteria. Mikrobiologiia 45, 512–514.
    [Google Scholar]
  30. Malofeeva, I. V., Bogorov, L. V. & Gogotov, I. N. ( 1974; ). Utilization of nitrates by purple bacteria. Mikrobiologiia 43, 967–972.
    [Google Scholar]
  31. Meincke, M., Bock, E., Kastrau, D. & Kroneck, P. M. H. ( 1992; ). Nitrite oxidoreductase from Nitrobacter hamburgensis: redox centers and their catalytic role. Arch Microbiol 158, 127–131.[CrossRef]
    [Google Scholar]
  32. Olmo-Mira, M. F., Cabello, P., Pino, C., Martínez-Luque, M., Richardson, D. J., Castillo, F., Roldán, M. D. & Moreno-Vivián, C. ( 2006; ). Expression and characterization of the assimilatory NADH-nitrite reductase from the phototrophic bacterium Rhodobacter capsulatus E1F1. Arch Microbiol 186, 339–344.[CrossRef]
    [Google Scholar]
  33. Olson, J. M. ( 1970; ). The evolution of photosynthesis. Science 168, 438–446.[CrossRef]
    [Google Scholar]
  34. Pfennig, N. ( 1967; ). Photosynthetic bacteria. Annu Rev Microbiol 21, 285–324.[CrossRef]
    [Google Scholar]
  35. Pfennig, N. ( 1976; ). Phototrophic green and purple bacteria: adaption to the aquatic environment and role in the sulfur cycle. Proc Soc Gen Microbiol 4, 19–20.
    [Google Scholar]
  36. Pfennig, N. ( 1977; ). Phototrophic green and purple bacteria: a comparative, systematic survey. Annu Rev Microbiol 31, 275–290.[CrossRef]
    [Google Scholar]
  37. Pfennig, N. ( 1978; ) General physiology and ecology of photosynthetic bacteria. In The Photosynthetic Bacteria, chapter 1, pp. 3–18. Edited by W. R. Sistrom & R. K. Clayton. New York: Plenum Press.
  38. Pfennig, N. & Biebl, H. ( 1976; ). Desulfuromonas acetoxidans gen. nov. and sp. nov., a new anaerobic, sulfur-reducing, acetate-oxidizing bacterium. Arch Microbiol 110, 3–12.[CrossRef]
    [Google Scholar]
  39. Pino, C., Olmo-Mira, F., Cabello, P., Martínez-Luque, M., Castillo, F., Roldán, M. D. & Moreno-Vivián, C. ( 2006; ). The assimilatory nitrate reduction system of the phototrophic bacterium Rhodobacter capsulatus E1F1. Biochem Soc Trans 34, 127–129.[CrossRef]
    [Google Scholar]
  40. Preuss, M. & Klemme, J.-H. ( 1983; ). Purification and characterization of a dissimilatory nitrite reductase from the phototrophic bacterium Rhodopseudomonas palustris. Z Naturforsch C 38, 933–938.
    [Google Scholar]
  41. Puchkova, N. N., Imhoff, J. F. & Gorlenko, V. M. ( 2000; ). Thiocapsa litoralis sp. nov., a new purple sulphur bacterium from microbial mats from the White Sea. Int J Syst Evol Microbiol 50, 1441–1447.[CrossRef]
    [Google Scholar]
  42. Satoh, T., Hoshino, Y. & Kitamura, H. ( 1976; ). Rhodopseudomonas sphaeroides forma sp. denitrificans, a denitrifying strain as a subspecies of Rhodopseudomonas sphaeroides. Arch Microbiol 108, 265–269.[CrossRef]
    [Google Scholar]
  43. Schaub, B. E. M. & van Gemerden, H. ( 1994; ). Simultaneous phototrophic and chemotrophic growth in the purple sulfur bacterium Thiocapsa roseopersicina M1. FEMS Microbiol Ecol 13, 185–196.[CrossRef]
    [Google Scholar]
  44. Siefert, E., Irgens, R. L. & Pfennig, N. ( 1978; ). Phototrophic purple and green bacteria in a sewage treatment plant. Appl Environ Microbiol 35, 38–44.
    [Google Scholar]
  45. Stackebrandt, E., Rainey, F. A. & Ward-Rainey, N. ( 1996; ). Anoxygenic phototrophy across the phylogenetic spectrum: current understanding and future perspectives. Arch Microbiol 166, 211–223.[CrossRef]
    [Google Scholar]
  46. Stanier, R. Y., Pfennig, N. & Trüper, H. G. ( 1981; ). Introduction to the phototrophic prokaryotes. In The Prokaryotes, chapter 7, pp. 197–211. Edited by M. P. Starr, H. Stolp, H. G. Trüper, A. Balows & H. G. Schlegel. Berlin, Heidelberg and New York: Springer Verlag.
  47. Stolz, J. F. & Basu, P. ( 2002; ). Evolution of nitrate reductase: molecular and structural variations on a common function. Chembiochem 3, 198–206.[CrossRef]
    [Google Scholar]
  48. Strohm, T. O., Griffin, B., Zumft, W. & Schink, B. ( 2007; ). Growth yields in bacterial denitrification and nitrate ammonification. Appl Environ Microbiol 73, 1420–1424.[CrossRef]
    [Google Scholar]
  49. Thauer, R. K., Jungermann, K. & Decker, K. ( 1977; ). Energy conservation in chemotrophic anaerobic bacteria. Bacteriol Rev 41, 100–180.
    [Google Scholar]
  50. Trüper, H. G. & Pfennig, N. ( 1981; ). Characterization and identification of the anoxygenic phototrophic bacteria. In The Prokaryotes, chapter 18, pp. 299–312. Edited by M. P. Starr, H. Stolp, H. G. Trüper, A. Balows & H. G. Schlegel. Berlin, Heidelberg and New York: Springer Verlag.
  51. Van Trappen, S., Mergaert, J. & Swings, J. ( 2004; ). Loktanella salsilacus gen. nov., sp. nov., Loktanella fryxellensis sp. nov. and Loktanella vestfoldensis sp. nov., new members of the Rhodobacter group, isolated from microbial mats in Antarctic lakes. Int J Syst Evol Microbiol 54, 1263–1269.[CrossRef]
    [Google Scholar]
  52. Visscher, P. T., Nijburg, J. W. & van Gemerden, H. ( 1990; ). Polysulfide utilization by Thiocapsa roseopersicina. Arch Microbiol 155, 75–81.[CrossRef]
    [Google Scholar]
  53. Weisburg, W. G., Barns, S. M., Pelletier, D. A. & Lane, D. J. ( 1991; ). 16S ribosomal DNA amplification for phylogenetic study. J Bacteriol 173, 697–703.
    [Google Scholar]
  54. Widdel, F. & Bak, F. ( 1992; ). Gram-negative mesophilic sulfate-reducing bacteria. In The Prokaryotes, pp. 3352–3378. Edited by A. Balows, H. G. Trüper, M. Dworkin, W. Harder & K.-H. Schleifer. New York: Springer.
  55. Widdel, F., Schnell, S., Heising, S., Ehrenreich, A., Aßmus, B. & Schink, B. ( 1993; ). Ferrous iron oxidation by anoxygenic phototrophic bacteria. Nature 362, 834–836.[CrossRef]
    [Google Scholar]
  56. Yildiz, F. H., Gest, H. & Bauer, C. E. ( 1991; ). Attenuated effect of oxygen on photopigment synthesis in Rhodospirillum centenum. J Bacteriol 173, 5502–5506.
    [Google Scholar]
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