Abstract
Three species of anoxygenic phototrophic heliobacteria, Heliobacterium chlorum, Heliobacterium gestii, and Heliobacillus mobilis, were studied for comparative nitrogen-fixing abilities and regulation of nitrogenase. Significant nitrogenase activity (acetylene reduction) was detected in all species grown photoheterotrophically on N2, although cells of H. mobilis consistently had higher nitrogenase activity than did cells of either H. chlorum or H. gestii. Nitrogen-fixing cultures of all three species of heliobacteria were subject to “switch-off” of nitrogenase activity by ammonia; glutamine also served to “switch-off” nitrogenase activity but only in cells of H. mobilis and H. gestii. Placing photosynthetically grown heliobacterial cultures in darkness also served to “switch-off” nitrogenase activity. Dark-mediated “switch-off” was complete in lactate-grown heliobacteria but in pyruvate-grown cells substantial rates of nitrogenase activity continued in darkness. In all heliobacteria examined ammonia was assimilated primarily through the glutamine synthetase/glutamate synthase (GS/GOGAT) pathway although significant levels of alanine dehydrogenase were present in extracts of cells of H. gestii, but not in the other species. The results suggest that heliobacteria, like phototrophic purple bacteria, are active N2-fixing bacteria and that despite their gram-positive phylogenetic roots, heliobacteria retain the capacity to control nitrogenase activity by a “switch-off” type of mechanism. Because of their ability to fix N2 both photosynthetically and in darkness, it is possible that heliobacteria are significant contributors of fixed nitrogen in their paddy soil habitat.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Beer-RomeroP, GestH (1987) Heliobacillus mobilis, a peritrichously flagellated anoxyphototroph containing bacteriochlorophyll g. FEMS Microbiol Lett 41: 109–114
BenderRA, JanssenKA, ResnickAD, BlumenbergM, FoorF, MagasanikB (1977) Biochemical parameters of glutamine synthetase from Klebsiella aerogenes. J Bacteriol 129: 1001–1009
BrownCM, HerbertRA (1977a) Ammonia assimilation in purple and green sulphur bacteria. FEMS Microbiol Lett 1: 39–42
BrownCM, HerbertRA (1977b) Ammonia assimilation in members of the Rhodospirillaceae. FEMS Microbiol Lett 1: 43–46
BureshRJ, CasselmanME, PatrickWHJr (1980) Nitrogen fixation in flooded soil systems, a review. Adv Agron 33: 149–192
GestH, FavingerJL (1983) Heliobacterium chlorum, an anoxygenic brownish-green photosynthetic bacterium containing a “new” form of bacteriochlorophyll. Arch Microbiol 136: 11–16
HabteM, AlexanderM (1980) Nitrogen fixation by photosynthetic bacteria in lowland rice culture. Appl Environ Microbiol 39: 342–347
HedaGD, MadiganMT (1986a) Aspects of nitrogen fixation in Chlorobium. Arch Microbiol 143: 330–336
HedaGD, MadiganMT (1986b) Utilization of amino acids and lack of diazotrophy in the thermophilic anoxygenic phototrophic bacterium Chloroflexus aurantiacus. J Gen Microbiol 132: 2469–2473
HedaGD, MadiganMT (1988) Nitrogen metabolism and N2 fixation in phototrophic green bacteria. In: OlsonJM, OrmerodJG, AmezJ, StackebrandtE, TrüperHG (eds) Green photosynthetic bacteria. Plenum Press, New York, pp 175–187
HongMM, ShenSC, BraunsteinAE (1959) Distribution of l-alanine dehydrogenase and l-glutamate dehydrogenase in Bacilli. Biochim Biophys Acta 36: 288–289
JohanssonBC, GestH (1976) Inorganic nitrogen assimilation by the photosynthetic bacterium Rhodopseudomonas capsulata. J Bacteriol 128: 683–688
KanemotoRH, LuddenPW (1984) Effect of ammonia, darkness, and phenazine methosulfate on whole-cell nitrogenase activity and Fe protein modification in Rhodospirillum rubrum. J Bacteriol 158: 713–720
KobayashiM, TakahashiE, KawaguchiE (1967) Distribution of nitrogen-fixing microorganisms in paddy soils of Southeast Asia. Soil Sci 104: 113–118
LoweryRG, LuddenPW (1988) Purification and properties of dinitrogenase reductase ADP-ribosyltransferase from the photosynthetic bacterium Rhodospirillum rubrum. J Biol Chem 263: 16714–16719
LuddenPW, BurrisRH (1981) In vivo and in vitro studies on ATP and electron donors to nitrogenase. Arch Microbiol 130: 155–158
LuddenPW, RobertsGP (1989) Regulation of nitrogenase activity by reversible ADP ribosylation. Curr Top Cell Regul 30: 23–55
MadiganMT (1988) Microbiology, physiology and ecology of anoxygenic phototrophic bacteria. In: ZehnderAJB (ed) Biology of anaerobic microorganisms. John Wiley and Sons, New York, pp 39–111
MadiganMT (1992) The family Heliobacteriaceae. In: BalowsA, TrüperHG; DworkinM, HarderW, SchleiferKH (eds) The prokaryotes, 2nd ed, Springer, Berlin Heidelberg New York, pp 1981–1992
MadiganMT, CoxSS (1982) Nitrogen metabolism in Rhodopseudomonas globiformis. Arch Microbiol 133: 6–10
MadiganMT, CoxSS, StegemanRA (1984) Nitrogen fixation and nitrogenase activities in members of the family Rhodospirillaceae. J Bacteriol 157: 73–78
MadiganMT, GestH (1979) Growth of the photosynthetic bacterium Rhodopseudomonas capsulata chemoautotrophically in darkness with H2 as the energy source. J Bacteriol 137: 524–530
MadiganMT, WallJD, GestH (1979) Dark anaerobic dinitrogen fixation by a photosynthetic microorganism. Science 204: 1429–1430
MastersRA, MadiganMT (1983) Nitrogen metabolism in the phototrophic bacteria Rhodocyclus purpureus and Rhodospirillum tenue. J Bacteriol 155: 222–227
MeersJL, TempestDW (1970) ‘Glutamine(amide): 2-oxoglutarate amino transferase oxidoreductase (NADP)’, an enzyme involved in the synthesis of glutamate by some bacteria. J Gen Microbiol 64: 187–194
Moreno-ViviánC, CejudoFJ, CárdenasH, CastilloF (1983) Ammonia assimilation pathways in Rhodopseudomonas capsulata E1F1. Arch Microbiol 136: 147–151
NeilsonAH, NordlundS (1975) Regulation of nitrogenase synthesis in intact cells of Rhodospirillum rubrum: inactivation of nitrogen fixation by ammonia, l-glutamine and l-asparagine. J Gen Microbiol 91: 53–62
OrmerodJ, NesbakkenT, TorgersenY (1990) Phototrophic bacteria that form heat resistant endospores. In: M.Baltscheffsky (ed) Current research in photosynthesis, vol 4. Kluwer, Academic Publishers, Dordrecht, The Netherlands, pp 935–938
PfennigN, TrüperHG (1989) Anoxygenic phototrophic bacteria. In: StaleyJT, BryantMP, PfennigN, HoltJG (eds) Bergey's manual of systematic bacteriology, vol 3. Williams and Wilkins, Baltimore, pp 1635–1709
RobertsGP, LuddenPW (1992) Nitrogen fixation by photosynthetic bacteria. In: StaceyG, BurrisRH, EvanHJ (eds) Biological nitrogen fixation. Chapman and Hall, New York
SchultzJE, GottoJW, WeaverPF, YochDC (1985) Regulation of nitrogen fixation in Rhodospirillum rubrum grown under dark, fermentative conditions. J Bacteriol 162: 1322–1324
ShapiroBM, StadtmanER (1970) Glutamine synthetase (Escherichia coli). In: TaborH, TaborCW (eds) Methods in enzymology, vol XVII. Metabolism of amino acids and amines, part A. Academic Press, New York, pp 910–922
WoeseCR, Debrunner-VossbrinckBA, OyaizuH, StackebrandtE, LudwigW (1985) Gram-positive bacteria: possible photosynthetic ancestry. Science 229: 762–765
WoeseCR (1987) Bacterial evolution. Microbiol Rev 51: 221–271
YoshidaA, FreeseE (1970) l-alanine dehydrogenase (Bacillus subtilis). In: TaborH, TaborCW (eds) Methods in enzymology, vol XVII. Metabolism of amino acids and amines, part A. Academic Press, New York, pp 176–181
ZumftWG, CastilloF (1978) Regulatory properties of the nitrogenase from Rhodopseudomonas palustris. Arch Microbiol 117: 53–60
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Kimble, L.K., Madigan, M.T. Nitrogen fixation and nitrogen metabolism in heliobacteria. Arch. Microbiol. 158, 155–161 (1992). https://doi.org/10.1007/BF00290810
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00290810