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. 1989 May;86(9):3399–3403. doi: 10.1073/pnas.86.9.3399

Differences in fatty acid composition between vegetative cells and N2-fixing vesicles of Frankia sp. strain CpI1

Anders Tunlid *,†, Nancy A Schultz ‡, David R Benson ‡, D Bernie Steele *, David C White *
PMCID: PMC287140  PMID: 16594036

Abstract

When growing on N2, actinomycetes from the genus Frankia form multicellular structures that contain nitrogenase. The structures are referred to as vesicles and are indistinguishable from vesicles formed when Frankia sp. are in root-nodule symbioses. Vesicles isolated from N2-grown cells of Frankia sp. strain CpI1 had a significantly higher amount and different composition of fatty acids than did vegetative cells recovered from NH4+-containing medium. Lipids from vesicles, whole cells grown on N2, and whole cells grown on NH4+ were fractionated by silicic acid chromatography into neutral lipids, glycolipids, and polar lipids. The fatty acids were transesterified by methanolysis and analyzed by gas chromatography and mass spectrometry. Vesicles had considerably higher amounts of fatty acids in the neutral and glycolipid fractions but lower amounts of polar lipid fatty acids than did vegetative cells. Polar lipids from vesicles had a higher proportion of mono-unsaturated and cyclopropane fatty acids and a lower proportion of isobranched fatty acids than did polar lipids from NH4+-grown or N2-grown cells. The neutral lipid and glycolipid fractions contained several long-chain compounds with molecular ions at m/z 408 and 410. The proportions of these compounds were significantly higher in the lipids from vesicles than from vegetative cells. These results suggest that lipids in vesicles might be involved in the protection of nitrogenase from O2 and suggest a parallel with the glycolipids involved in protecting nitrogenase from O2 in the cyanobacterial heterocysts.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. BLIGH E. G., DYER W. J. A rapid method of total lipid extraction and purification. Can J Biochem Physiol. 1959 Aug;37(8):911–917. doi: 10.1139/o59-099. [DOI] [PubMed] [Google Scholar]
  2. Benson D. R., Arp D. J., Burris R. H. Cell-free nitrogenase and hydrogenase from actinorhizal root nodules. Science. 1979 Aug 17;205(4407):688–689. doi: 10.1126/science.205.4407.688. [DOI] [PubMed] [Google Scholar]
  3. Boon J. J., van de Graaf B., Schuyle P. J., de Lange F., de Leeuw J. W. The mass spectrometry of iso and anteiso monoenoic fatty acids. Lipids. 1977 Sep;12(9):717–721. doi: 10.1007/BF02570901. [DOI] [PubMed] [Google Scholar]
  4. Callaham D., Deltredici P., Torrey J. G. Isolation and Cultivation in vitro of the Actinomycete Causing Root Nodulation in Comptonia. Science. 1978 Feb 24;199(4331):899–902. doi: 10.1126/science.199.4331.899. [DOI] [PubMed] [Google Scholar]
  5. Cronan J. E., Jr, Gelmann E. P. Physical properties of membrane lipids: biological relevance and regulation. Bacteriol Rev. 1975 Sep;39(3):232–256. doi: 10.1128/br.39.3.232-256.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Fulco A. J. Fatty acid metabolism in bacteria. Prog Lipid Res. 1983;22(2):133–160. doi: 10.1016/0163-7827(83)90005-x. [DOI] [PubMed] [Google Scholar]
  7. Gauthier D., Diem H. G., Dommergues Y. In vitro nitrogen fixation by two actinomycete strains isolated from casuarina nodules. Appl Environ Microbiol. 1981 Jan;41(1):306–308. doi: 10.1128/aem.41.1.306-308.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Haury J. F., Wolk C. P. Classes of Anabaena variabilis mutants with oxygen-sensitive nitrogenase activity. J Bacteriol. 1978 Nov;136(2):688–692. doi: 10.1128/jb.136.2.688-692.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. King J. D., White D. C., Taylor C. W. Use of lipid composition and metabolism to examine structure and activity of estuarine detrital microflora. Appl Environ Microbiol. 1977 May;33(5):1177–1183. doi: 10.1128/aem.33.5.1177-1183.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Lambein F., Wolk C. P. Structural studies on the glycolipids from the envelope of the heterocyst of Anabaena cylindrica. Biochemistry. 1973 Feb 27;12(5):791–798. doi: 10.1021/bi00729a002. [DOI] [PubMed] [Google Scholar]
  11. McCloskey J. A., Law J. H. Ring location in cyclopropane fatty acid esters by a mass spectrometric method. Lipids. 1967 May;2(3):225–230. doi: 10.1007/BF02532560. [DOI] [PubMed] [Google Scholar]
  12. Murry M. A., Fontaine M. S., Tjepkema J. D. Oxygen protection of nitrogenase in Frankia sp. HFPArI3. Arch Microbiol. 1984 Oct;139(2-3):162–166. doi: 10.1007/BF00401993. [DOI] [PubMed] [Google Scholar]
  13. Murry M. A., Zhongze Z., Torrey J. G. Effect of O2 on vesicle formation, acetylene reduction, and O2-uptake kinetics in Frankia sp. HFPCcI3 isolated from Casuarina cunninghamiana. Can J Microbiol. 1985 Sep;31(9):804–809. doi: 10.1139/m85-151. [DOI] [PubMed] [Google Scholar]
  14. Newcomb W., Wood S. M. Morphogenesis and fine structure of Frankia (Actinomycetales): the microsymbiont of nitrogen-fixing actinorhizal root nodules. Int Rev Cytol. 1987;109:1–88. doi: 10.1016/s0074-7696(08)61719-2. [DOI] [PubMed] [Google Scholar]
  15. Noridge N. A., Benson D. R. Isolation and nitrogen-fixing activity of Frankia sp. strain CpI1 vesicles. J Bacteriol. 1986 Apr;166(1):301–305. doi: 10.1128/jb.166.1.301-305.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Parsons R., Silvester W. B., Harris S., Gruijters W. T., Bullivant S. Frankia vesicles provide inducible and absolute oxygen protection for nitrogenase. Plant Physiol. 1987 Apr;83(4):728–731. doi: 10.1104/pp.83.4.728. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. RYHAGE R., STENHAGEN E. Mass spectrometry in lipid research. J Lipid Res. 1960 Oct;1:361–390. [PubMed] [Google Scholar]
  18. SCHEURBRANDT G., BLOCH K. Unsaturated fatty acids in microorganisms. J Biol Chem. 1962 Jul;237:2064–2068. [PubMed] [Google Scholar]
  19. Stewart W. D. Some aspects of structure and function in N2-fixing cyanobacteria. Annu Rev Microbiol. 1980;34:497–536. doi: 10.1146/annurev.mi.34.100180.002433. [DOI] [PubMed] [Google Scholar]
  20. Tisa L. S., Ensign J. C. Isolation and nitrogenase activity of vesicles from Frankia sp. strain EAN1pec. J Bacteriol. 1987 Nov;169(11):5054–5059. doi: 10.1128/jb.169.11.5054-5059.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]

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