Skip to main content
PMC home page
Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1990 Oct;87(19):7565–7569. doi: 10.1073/pnas.87.19.7565

Sterol phylogenesis and algal evolution.

W D Nes 1, R A Norton 1, F G Crumley 1, S J Madigan 1, E R Katz 1
PMCID: PMC54788  PMID: 11607106

Abstract

The stereochemistry of several sterol precursors and end products synthesized by two fungal-like micro-organisms Prototheca wickerhamii (I) and Dictyostelium discoideum (II) have been determined by chromatographic (TLC, GLC, and HPLC) and spectral (UV, MS, and 1H NMR) methods. From I and II the following sterols were isolated from the cells: cycloartenol, cyclolaudenol, 24(28)-methylenecycloartanol, ergosterol, protothecasterol, 4alpha-methylergostanol, 4alpha-methylclionastanol, clionastanol, 24beta-ethylcholesta-8,22-enol, and dictyosterol. In addition, the mechanism of C-24 methylation was investigated in both organisms by feeding to I [2-3H]lanosterol, [2-3H]cycloartenol, [24-3H]lanosterol, and [methyl-2H3]methionine and by feeding to II [methyl-2H3]methionine. The results demonstrate that the 24beta configuration is formed by different alkylation routes in I and II. The Delta25(27) route operates in I while the Delta24(28) route operates in II. Based on what is known in the literature regarding sterol distribution and phylogenesis together with our findings that the stereochemical outcome of squalene oxide cyclization leads to the production of cycloartenol rather than lanosterol (characteristic of the fungal genealogy) and the chirality of the C-24 alkyl group is similar in the two nonphotosynthetic microbes (beta oriented), we conclude that Prototheca is an apoplastic Chlorella (i.e., an alga) and that Dictyostelium as well as the other soil amoebae that synthesize cycloartenol evolved from algal rather than fungal ancestors.

Full text

PDF
7565

Selected References

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

  1. Adler J. H., Young M., Nes W. R. Determination of the absolute configuration at C-20 and C-24 of ergosterol in Ascomycetes and Basidiomycetes by proton magnetic resonance spectroscopy. Lipids. 1977 Apr;12(4):364–366. doi: 10.1007/BF02533639. [DOI] [PubMed] [Google Scholar]
  2. Adolph E. F. The heart's pacemaker. Sci Am. 1967 Mar;216(3):32–37. doi: 10.1038/scientificamerican0367-32. [DOI] [PubMed] [Google Scholar]
  3. Akihisa T., Matsubara Y., Ghosh P., Thakur S., Tamura T., Matsumoto T. Sterols of some Clerodendrum species (Verbenaceae): occurrence of the 24 alpha- and 24 beta-epimers of 24-ethylsterols lacking a delta 25-bond. Steroids. 1989 Mar-May;53(3-5):625–638. doi: 10.1016/0039-128x(89)90036-6. [DOI] [PubMed] [Google Scholar]
  4. Anding C., Brandt R. D., Ourisson G. Sterol biosynthesis in Euglena gracilis Z. Sterol precursors in light-grown and dark-grown Euglena gracilis Z. Eur J Biochem. 1971 Dec;24(2):259–263. doi: 10.1111/j.1432-1033.1971.tb19679.x. [DOI] [PubMed] [Google Scholar]
  5. Cavalier-Smith T. The origin of eukaryotic and archaebacterial cells. Ann N Y Acad Sci. 1987;503:17–54. doi: 10.1111/j.1749-6632.1987.tb40596.x. [DOI] [PubMed] [Google Scholar]
  6. Ellouz R., Lenfant M. Biosynthèse de la chaîne latérale éthyle du stigmastanol et du stigmastèn-22,01-3beta du myxomycète Dictyostelium discoïdeum. Eur J Biochem. 1971 Dec 10;23(3):544–550. doi: 10.1111/j.1432-1033.1971.tb01652.x. [DOI] [PubMed] [Google Scholar]
  7. Field K. G., Olsen G. J., Lane D. J., Giovannoni S. J., Ghiselin M. T., Raff E. C., Pace N. R., Raff R. A. Molecular phylogeny of the animal kingdom. Science. 1988 Feb 12;239(4841 Pt 1):748–753. doi: 10.1126/science.3277277. [DOI] [PubMed] [Google Scholar]
  8. Goad L. J., Holz G. G., Jr, Beach D. H. Sterols of Leishmania species. Implications for biosynthesis. Mol Biochem Parasitol. 1984 Feb;10(2):161–170. doi: 10.1016/0166-6851(84)90004-5. [DOI] [PubMed] [Google Scholar]
  9. Goad L. J., Lenton J. R., Knapp F. F., Goodwin T. W. Phytosterol side chain biosynthesis. Lipids. 1974 Aug;9(8):582–595. doi: 10.1007/BF02532508. [DOI] [PubMed] [Google Scholar]
  10. Gunderson J. H., Elwood H., Ingold A., Kindle K., Sogin M. L. Phylogenetic relationships between chlorophytes, chrysophytes, and oomycetes. Proc Natl Acad Sci U S A. 1987 Aug;84(16):5823–5827. doi: 10.1073/pnas.84.16.5823. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. HEFTMANN E., WRIGHT B. E., LIDDEL G. U. The isolation of Delta22-stigmasten-3beta-ol from Dictyostelium discoideum. Arch Biochem Biophys. 1960 Dec;91:266–270. doi: 10.1016/0003-9861(60)90500-2. [DOI] [PubMed] [Google Scholar]
  12. Halevy S., Avivi L., Katan H. Sterols of soil amoebas and Ochromonas danica: phylogenetic approach. J Protozool. 1966 Aug;13(3):480–483. doi: 10.1111/j.1550-7408.1966.tb01945.x. [DOI] [PubMed] [Google Scholar]
  13. Kerfin W., Kessler E. Physiological and biochemical contributions to the taxonomy of the genus Prototheca. II. Starch hydrolysis and base composition of DNA. Arch Microbiol. 1978 Jan 23;116(1):105–107. doi: 10.1007/BF00408740. [DOI] [PubMed] [Google Scholar]
  14. Lenfant M., Ellouz R., Das B. C., Zissmann E., Lederer E. Sur la biosynthèse de la chaîne latérale éthyle des stérols du Myxomycète Dictyostelium discoideum. Eur J Biochem. 1969 Jan;7(2):159–164. doi: 10.1111/j.1432-1033.1969.tb19587.x. [DOI] [PubMed] [Google Scholar]
  15. Levine N. D., Corliss J. O., Cox F. E., Deroux G., Grain J., Honigberg B. M., Leedale G. F., Loeblich A. R., 3rd, Lom J., Lynn D. A newly revised classification of the protozoa. J Protozool. 1980 Feb;27(1):37–58. doi: 10.1111/j.1550-7408.1980.tb04228.x. [DOI] [PubMed] [Google Scholar]
  16. Malhotra H. C., Nes W. R. The conversion of mevalonate to 24-methylenecycloartanol by a cell-free enzyme preparation from nonphotosynthetic tissue. J Biol Chem. 1972 Oct 10;247(19):6243–6246. [PubMed] [Google Scholar]
  17. Nes W. D., Stafford A. E. Evidence for metabolic and functional discrimination of sterols by Phytophthora cactorum. Proc Natl Acad Sci U S A. 1983 Jun;80(11):3227–3231. doi: 10.1073/pnas.80.11.3227. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Nes W. R. Role of sterols in membranes. Lipids. 1974 Aug;9(8):596–612. doi: 10.1007/BF02532509. [DOI] [PubMed] [Google Scholar]
  19. Ourisson G., Rohmer M., Poralla K. Prokaryotic hopanoids and other polyterpenoid sterol surrogates. Annu Rev Microbiol. 1987;41:301–333. doi: 10.1146/annurev.mi.41.100187.001505. [DOI] [PubMed] [Google Scholar]
  20. Perasso R., Baroin A., Qu L. H., Bachellerie J. P., Adoutte A. Origin of the algae. Nature. 1989 May 11;339(6220):142–144. doi: 10.1038/339142a0. [DOI] [PubMed] [Google Scholar]
  21. Raederstorff D., Rohmer M. Sterol biosynthesis de nova via cycloartenol by the soil amoeba Acanthamoeba polyphaga. Biochem J. 1985 Nov 1;231(3):609–615. doi: 10.1042/bj2310609. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Raederstorff D., Rohmer M. Sterol biosynthesis via cycloartenol and other biochemical features related to photosynthetic phyla in the amoeba Naegleria lovaniensis and Naegleria gruberi. Eur J Biochem. 1987 Apr 15;164(2):427–434. doi: 10.1111/j.1432-1033.1987.tb11075.x. [DOI] [PubMed] [Google Scholar]
  23. Rohmer M., Brandt R. D. Les stèrols et leurs prècurseurs chez Astasia longa Pringsheim. Eur J Biochem. 1973 Jul 16;36(2):446–454. doi: 10.1111/j.1432-1033.1973.tb02929.x. [DOI] [PubMed] [Google Scholar]
  24. Schopf J. W. The evolution of the earliest cells. Sci Am. 1978 Sep;239(3):110-2, 114, 116-20 passim. doi: 10.1038/scientificamerican0978-110. [DOI] [PubMed] [Google Scholar]
  25. Whittaker R. H. New concepts of kingdoms or organisms. Evolutionary relations are better represented by new classifications than by the traditional two kingdoms. Science. 1969 Jan 10;163(3863):150–160. doi: 10.1126/science.163.3863.150. [DOI] [PubMed] [Google Scholar]
  26. Williams B. L., Goodwin T. W., Ryley J. F. The sterol content of some protozoa. J Protozool. 1966 May;13(2):227–230. doi: 10.1111/j.1550-7408.1966.tb01898.x. [DOI] [PubMed] [Google Scholar]
  27. Xu S. H., Norton R. A., Crumley F. G., Nes W. D. Comparison of the chromatographic properties of sterols, select additional steroids and triterpenoids: gravity-flow column liquid chromatography, thin-layer chromatography, gas-liquid chromatography and high-performance liquid chromatography. J Chromatogr. 1988 Oct 28;452:377–398. doi: 10.1016/s0021-9673(01)81462-x. [DOI] [PubMed] [Google Scholar]

Articles from Proceedings of the National Academy of Sciences of the United States of America are provided here courtesy of National Academy of Sciences

RESOURCES