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Biomacromolecules of algae and plants and their fossil analogues

Chapter
Part of the Tasks for vegetation science book series (TAVS, volume 41)

Abstract

A review of our current understanding of resistant biomacromolecules derived from present and past algae and higher plants is presented. Insight in the nature of recent and fossil macromolecules is strongly hampered by the difficulties in obtaining the material in pure and unaltered form. For the extant material, avoiding artificial condensation and structural alteration as a result of chemical isolation and purification of biomacromolecules requires constant attention. To date, several types of sporopollenin seem to occur. One type is characterised by oxygenated aromatic building blocks, in particular p-coumaric acid and ferrulic acid. The other type is thought to consist predominantly of an aliphatic biopolymer. In this review it is concluded that extant sporopollenin consists of the aromatic type, whereas the aliphatic component of fossil sporopollenin is due to early-diagenetic oxidative polymerization of unsaturated lipids. The cuticles of most higher plants contain the aliphatic biopolyester cutin. Additionally, cuticles of drought-adapted, mostly CAM plants, seem to contain the non-hydrolysable aliphatic biopolymer cutan. Only a very few algae are able to biosynthesize resistant, (fossilisable) cell walls: some Chlorophyta, Eustigmatophyta and Prasinophyta produce the aliphatic biopolymer algaenan. Some Dinophyta are also capable of producing algaenan cell walls. Additionally, some taxa produce highly resistant cyst-walls with a high proportion of aromatic moieties. For the morphologically well-preserved fossil material, contamination by organic particles other than the target taxon is hard to eliminate and can contribute to either the aliphatic or aromatic signal. Furthermore, post-mortem migration of aliphatic moieties into, and their condensation onto the macromolecule might occur, e.g. by oxidative polymerization. These phenomena hamper the evaluation of the aliphatic signature of fossil plant material and may for example explain the preservation of initially cutin-based cuticles or non-algaenan containing algae. The extent to which migration and in situ formation of aromatic moieties plays a role in modifying resistant algal macromolecules, notably under elevated temperature and/or pressure conditions, still remains an open question.

Key words

Algaenan Biomacromolecule Diagenesis Fossil Recent Sporopollenin 

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References

  1. Aken M.E. and Pienaar R.N. 1985. Preliminary investigations on the chemical composition of the scale-boundary and cyst wall of Pyramimonas pseudoparkeae (Prasinophyceae). S. Afr. J. Bot. 51: 408–416.Google Scholar
  2. Allard B. and Templier J. 2000. Comparison of neutral lipid profile of various trilaminar outer cell wall (TLS)-containing microalgae with emphasis on algaenan occurrence. Phytochemistry 54: 369–380.PubMedGoogle Scholar
  3. Allard B. and Templier J. 2001. High molecular weight lipids from the trilaminar outer wall (TLS)-containing microalgae Chlorella emersonii, Scenedesmus communis and Tetraedron minimum. Phytochemistry 57: 459–467.PubMedGoogle Scholar
  4. Allard B., Templier J. and Largeau C. 1998. An improved method for the isolation of artifact-free algaenans from microalgae. Org. Geochem. 28: 543–548.Google Scholar
  5. Arouri K., Greenwood P.F. and Walter M.R. 1999. A possible chlorophycean affinity of some Neoproterozoic acritarchs. Org. Geochem. 30: 1323–1337.Google Scholar
  6. Arouri K.R., Greenwood P.F. and Walter M.R. 2000. Biological affinities of Neoproterozoic acritarchs from Australia: microscopic and chemical characterisation. Org. Geochem. 31: 75–89.Google Scholar
  7. Ashraf M. and Godward M.B.E. 1980. Ultrastructure and chemistry of the zygospore wall of Spirogyra. Ann. Bot. 46: 485–487.Google Scholar
  8. Atkinson A.W. Jr, Gunning B.E.S. and John P.C.L. 1972. Sporopollenin in the cell wall of Chlorella and other algae: ultrastructure, chemistry and incorporation of 14C-acetate, studied in synchronous cultures. Planta 107: 1–32.Google Scholar
  9. Batten D.J. 1996. Green and blue-green algae. Colonial Chlorococcales. In: Jansonius J. and McGregor D.C. (eds.), Palynolog: Principles and Applications, AASP Foundation, Salt Lake City, pp. 191–203.Google Scholar
  10. Batten D.J. and Grenfell H.R. 1996. Green and blue-green algae. Botryococcus. In: Jansonius J. and McGregor D.C. (eds.), Palynology: Principles and Applications, AASP Foundation, Salt Lake City, pp. 205–214.Google Scholar
  11. Berkaloff C., Casadevall E., Largeau C., Metzger P., Peracca S. and Virlet J. 1983. The resistant polymer of the walls of the hydrocarbon-rich alga Botryococcus braunii. Phytochemistry 22: 389–397.Google Scholar
  12. van Bergen P.F. 1994. Palaeobotany of Propagules: An Investigation combining Microscopy and Chemistry. Ph.D. Thesis. University of London, London.Google Scholar
  13. van Bergen P.F., Blokker P., Collinson M.E., Sinninghe Damsté J.S. and de Leeuw J.W. 2004. Structural biomacromolecules in plants. What can be learnt from the fossil record?. In: Hemsley A.R. and Poole I. (eds.), Evolution of Plant Physiology, Elsevier, Amsterdam, pp. 133–154.Google Scholar
  14. van Bergen P.F., Collinson M.E., Blokker P., Van Moerkerken P., Barrie P.J. and de Leeuw J.W. Chemical characterization of (fossil) sporopollenin: a molecular comparison of Azolla microspore massulae and Kurtzipites pollen with a review of previous literature, in press.Google Scholar
  15. van Bergen P.F., Collinson M.E., Briggs D.E.G., de Leeuw J.W., Scott A.C., Evershed R.P. and Finch P. 1995. Resistant biomacromolecules in the fossil record. Acta Bot. Neerl. 44: 319–345.Google Scholar
  16. van Bergen P.F., Collinson M.E. and de Leeuw J.W. 1993. Chemical composition and ultrastructure of fossil and extant salvinialean microspore massulae and megaspores. Grana Suppl. 1: 18–30.Google Scholar
  17. Bertheas O., Metzger P. and Largeau C. 1999. A high molecular weight complex lipid, aliphatic polyaldehyde tetraterpenediol polyacetal from Botryococcus braunii (L. race). Phytochem. 50: 85–96.Google Scholar
  18. Biedlingmaier S., Wanner G. and Schmidt A. 1987. A correlation between detergent tolerance and cell wall structure in green algae. Z. Naturforsch. 42: 245–250.Google Scholar
  19. Binder B.J. and Anderson D.M. 1990. Biochemical composition and metabolic activity of Scripsiella trochoidea (Dinophyceae) resting cysts. J. Phycol. 26: 289–298.Google Scholar
  20. Blokker P. 2000. Structural analysis of resistant polymers in extant algae and ancient sediments. Geol. Ultratrajectina 193: 1–145.Google Scholar
  21. Blokker P., Schouten S., de Leeuw J.W., Sinninghe Damsté J.S. and van den Ende H. 1999. Molecular structure of the resistant biopolymer in the zygospore cell walls of Chlamydomonas monoica. Planta 207: 539–543.Google Scholar
  22. Blokker P., Schouten S., de Leeuw J.W., Sinninghe Damsté J.S. and van den Ende H. 2000. A comparitive study of fossil and extant algaenans using ruthenium tetroxide degradation. Geochim. Cosmochim. Acta 64: 2055–2065.Google Scholar
  23. Blokker P., Schouten S., van den Ende H., de Leeuw J.W., Hatcher P.G. and Sinninghe Damsté J.S. 1998a. Chemical structure of algaenans from the fresh water algae Tetraedron minimum, Scenedesmus communis and Pediastrum boryanum. Org. Geochem. 29: 1453–1468.Google Scholar
  24. Blokker P., Schouten S., van den Ende H., de Leeuw J.W. and Sinninghe Damsté J.S. 1998b. Cell wall specific ω-hydroxy fatty acids in freshwater green microalgae. Phytochem. 49: 691–695.Google Scholar
  25. Blokker P., van Bergen P., Pancost R., Collinson M.E., de Leeuw J.W. and Sinninghe Damsté J.S. 2001. The chemical structure of Gloeocapsamorpha prisca microfossils: Implications for their origin. Geochim. Cosmochim. Acta 65: 885–900.Google Scholar
  26. Blom A.V. 1936. Quelques remarques sur le mé canisme de séchage des peintures à l’huile. Peintures, Pigments, Vernis 13: 156–162.Google Scholar
  27. Boom A. 2004. A Geochemical Study of Lacustrine Sediments: Towards Palao-climatic Econstructions of HighAndean Biomes in Colombia. University of Amsterdam, Amsterdam, p. 125.Google Scholar
  28. Boom A., Sinninghe Damsté J.S. and de Leeuw J.W. 2005. Cutan, a common aliphatic biopolymer in cuticles of drought-adapted plants. Org. Geochem. 36: 596–601.Google Scholar
  29. Briggs D.E.G., Kear A.J., Baas M., de Leeuw J.W. and Rigby S. 1995. Decay and composition of the hemichordate Rhabdopleura: implications for the taphonomy of graptolites. Lethaia 28: 15–23.Google Scholar
  30. Brunner U. and Honegger R. 1985. Chemical and ultrastructural studies on the distribution of sporopollenin like biopolymers in six genera of lichen phycobionts. Can. J. Bot. 63: 2221–2230.Google Scholar
  31. Burczyk J. 1987a. Biogenic relationships between ketocarotenoids and sporopollenins in green algae. Phytochemistry 26: 113–119.Google Scholar
  32. Burczyk J. 1987b. Cell wall carotenoids in green algae which form sporopollenins. Phytochemistry 26: 121–128.Google Scholar
  33. Burczyk J., Šmietana B., Terminska-Pabis K., Zych M. and Kowalowski P. 1999. Comparison of nitrogen content amino acid composition and glucosamine content of cell walls of various chlorococcalean algae. Phytochemistry 51: 491–497.Google Scholar
  34. Butterfield N.J. and Rainbird R.H. 1998. Diverse organic-walled fossils, including ‘possible dinoflagellates’ from the early Neoproterozoic of arctic Canada. Geology 26: 963–966.Google Scholar
  35. Collinson M.E., Mösle B., Finch P., Scott A.C. and Wilson R. 1998. Structure, biosynthesis and biodegradation of cutin and suberin. Ancient Biomol. 2: 251–265.Google Scholar
  36. Collinson M.E. and van Bergen P.F. 2004. Evolution of angiosperm fruit and seed physiology: anatomical and chemical evidence from fossils. In: Hemsley A.R. and Poole I. (eds.), Evolution of Plant Physiology, Elsevier, Amsterdam, pp. 343–377.Google Scholar
  37. Collinson M.E., van Bergen P.F., Scott A.C. and de Leeuw J.W. 1994. The oil-generating potential of plants from coal and coal-bearing strata through time: a review with new evidence from Carboniferous plants. Geol. Soc. Spec. Publ. 77: 31–70.Google Scholar
  38. Combaz A. 1971. Themal degradation of sporopollenin and genesis of hydrocarbons. In: Brooks J. (ed.), Sporopollenin, Academic Press, London, pp. 621–653.Google Scholar
  39. Corre G., Templier J., Largeau C., Rousseau B. and Berkaloff C. 1996. Influence of cell wall composition on the resistance of two Chlorella species (Chlorophyta) to detergents. J. Phycol. 32: 584–590.Google Scholar
  40. Dale B. 1976. Cyst formation, sedimentation, and preservation: factors affecting dinoflagellate assemblages in recent sediments from Trondheimsfjord. Norway. Rev. Palaeobot. Palynol. 22: 39–60.Google Scholar
  41. Dammers N. 2003. Chemical characterization of the organicwalled dinoflagellate cyst taxa Nematosphaeropsis labyrinthus, Polysphaeridium zoharii, Brigantedinium spp. and Palaeoperidinium spp. and a review on algaenan and dinosterol. Masters Thesis, Department of Geochemistry, Utrecht University, 43 pp.Google Scholar
  42. de Leeuw J.W. and Largeau C. 1993. A review of macromolecular compounds that comprise living organisms and their role in kerogen, coal and petroleum formation. In: Engel M.H. and Macko S.A. (eds.), Organic Geochemistry. Principles and Applications, Plenum Press, New York, pp. 23–72.Google Scholar
  43. de Vries P.J.R., Simons J. and van Beem A.P. 1983. Sporopollenin in the spore wall of Spirogyra (Zygnemataceae, Chlorophyceae). Acta Bot. Neerl. 32: 252–258.Google Scholar
  44. Derenne S., Largeau C. and Behar F. 1994. Low polarity pyrolysis products of Permian to Recent Botryoccus-rich sediments: first evidence for the contribution of an isoprenoid algaenan to kerogen formation. Geochim. Cosmochim. Acta 58: 3703–3711.Google Scholar
  45. Derenne S., Largeau C. and Berkaloff C. 1996. First example of an algaenan yielding an aromatic-rich pyrolysate. Possible geochemical implications on marine kerogen formation. Org. Geochem. 24: 617–627.Google Scholar
  46. Derenne S., Largeau C., Berkaloff C., Rousseau B., Wilhelm C. and Hatcher P.G. 1992a. Non-hydrolysable macromolecular constituents from outer walls of Chlorella fusca and Nanochlorum eucaryotum. Phytochemistry 31: 1923–1929.Google Scholar
  47. Derenne S., Largeau C., Casadevall E., Berkaloff C. and Rousseau B. 1991. Chemical evidence of kerogen formation in source rocks and oil shales via selective preservation of thin resistant outer walls of microalgae: origin of ultralaminae. Geochim. Cosmochim. Acta 55: 1041–1050.Google Scholar
  48. Derenne S., Largeau C., Hetényi M., Brukner-Wein A., Conan J. and Lugardon B. 1997. Chemical structure of the organic matter in a Pliocene maar-type shale: implicated Botryococcus race strains and formation pathways. Geochim. Cosmochim. Acta 61: 1879–1889.Google Scholar
  49. Derenne S., Metzger P., Largeau C., van Bergen P.F., Gatellier J.P., Sinninghe Damsté J.S., de Leeuw J.W. and Berkaloff C. 1992. Similar morphological and chemical variations of Gloeocapsomorpha prisca in Ordovician sediments and cultured Botryococcus braunii as a response to changes in salinity. Org. Geochem. 19: 299–313.Google Scholar
  50. Deshmukh A.P., Simpson A.J. and Hatcher P.G. 1964. Evidence for cross-linking in tomato cutin using HR-MAS NMR spectroscopy. Phytochemistry 64: 1163–1170.Google Scholar
  51. Domínguez E., Mercado J.A., Quesada M.A. and Heredia A. 1999. Pollen sporopollenin: degradation and structural elucidation. Sex. Plant Reprod. 12: 171–178.Google Scholar
  52. Fensome R.A., et al., 1993. A Classification of Modern and Fossil Dinoflagellates. Sheridan Press, Hanover, p. 351.Google Scholar
  53. Fensome R.A., Saldarriaga J.F. and Taylor F.J.R. 1999. Dinoflagellate phylogeny revisited: reconciling morphological and molecular based phylogenies. Grana 38: 66–80.Google Scholar
  54. Fjällström P., Andersson B., Nilsson C. and Andersson K. 2002. Drying of linseed oil paints: a laboratory study of aldehyde emissions. Indust. Crop. Prod. 16: 173–184.Google Scholar
  55. Foster C.B., Stephenson M.H., Marshall C., Logan G.A. and Greenwood P.F. 2002. A revision of Reduviasporonites Wilson 1962: description, illustration, comparison and biological affinities. Palynology 26: 35–58.Google Scholar
  56. Gabarayeva N.I., Blackmore S. and Rowley J.R. 2003. Observations on the experimental destruction and substructural organisation of the pollen wall of some selected Gymnosperms and Angiosperms. Rev. Palaeobot. Palynol. 124: 203–226.Google Scholar
  57. van Geel B. and Grenfell H.R. 1996. Green and blue-green algae. Spores of Zygnemataceae. In: Jansonius J. and McGregor D.C. (eds.), Palynology: Principles and Applications, AASP Foundation, Salt Lake City, pp. 173–179.Google Scholar
  58. Gelin F., Boogers I., Noordeloos A.A.M., Sinninghe Damsté J.S., Riegman R. and de Leeuw J.W. 1997. Resistant biomacromolecules in marine microalgae of the classes Eustigmatophyceae and Chlorophyceae: Geochemical applications. Org. Geochem. 26: 659–675.Google Scholar
  59. Gelin F., Volkman J.K., Largeau C., Derenne S., Sinninghe Damsté J.S. and de Leeuw J.W. 1999. Distribution of aliphatic nonhydrolyzable biopolymers in marine microalgae. Org. Geochem. 30: 147–159.Google Scholar
  60. Good B.H. and Chapman R.L. 1978. The ultrastructure of Phycopeltis (Chroolepidaceae: Chlorophyta). I. Sporopollenin in the cell walls. Am. J. Bot. 65: 27–33.Google Scholar
  61. Goth K., de Leeuw J.W., Püttmann W. and Tegelaar E.W. 1988. Origin of messel oil shale kerogen. Nature 336: 759–761.Google Scholar
  62. Gray J. and Boucot A.J. 1989. Is Moyeria a euglenoid?. Lethaia 22: 447–456.Google Scholar
  63. Greenwood P.F., Arouri K.R. and George S.C. 2000. Tricyclic terpenoid composition of Tasmanites kerogen as determined by pyrolysis GC-MS. Geochim. Cosmochim. Acta 64: 1249–1263.Google Scholar
  64. Guilford W.J., Schneider D.M., Labovitz J. and Opella S.J. 1988. High resolution solid state 13C NMR spectroscopy of sporopollenin from different plant taxa. Plant Physiol. 86: 134–136.PubMedGoogle Scholar
  65. Gunnison D. and Alexander M. 1975. Basis for the resistance of several algae to microbial decomposition. Appl. Microbiol. 29: 729–738.PubMedGoogle Scholar
  66. Guy-Ohlson D. 1996. Green and blue-green algae. Prasinophyceanalgae. In: Jansonius J. and McGregor D.C. (eds.), Palynology: Principles and Applications, AASP Foundation, Salt Lake City, pp. 181–189.Google Scholar
  67. Hartgers W.A., Sinninghe Damsté J.S. and de Leeuw J.W. 1995. Curie-point pyrolysis of sodium salts of functionalized fatty acids. J. Anal. Appl. Pyrolysis 34: 191–217.Google Scholar
  68. Hayatsu R., Botto R.E., Mcbeth R.L., Scott R.G. and Winans R.E. 1988. Chemical alteration of a biological polymer’ sporopollenin’ during coalification: origin, formation, and transformation of the coal maceral sporinite. Energy Fuel 2: 843–847.Google Scholar
  69. Hegewald E. and Deason T.R. 1988. Pseudoschroederia punctata (Chlorophyta, Chlorococcales), a new species with an unusual cell wall. Arch. Hydrobiol. Suppl. 78: 465–473.Google Scholar
  70. Hegewald E. and Deason T.R. 1989. Pseudodidymocystis, a new genus of Scenedesmaceae (Chlorophyceae). Arch. Hydrobiol. Suppl. 82: 119–127.Google Scholar
  71. Hemsley A.R., Barrie P.J., Chaloner W.G. and Scott A.C. 1993. The composition of sporopollenin and its use in living and fossil plant systematics. Grana Suppl. 1: 2–11.Google Scholar
  72. Hemsley A.R., Barrie P.J. and Chaloner W.G. 1994. Studies of fossil and modern spore and pollen wall biomacromolecules using 13C solid state NMR. NERC Spec. Publ. 94: 15–19.Google Scholar
  73. Holloway P.J. 1982. The chemical constitution of plant cutins. In: Cutler D.F. (ed.), The Plant Cuticle, Elsevier, Amsterdam, pp. 45–85.Google Scholar
  74. Honegger R. and Brunner U. 1981. Sporopollenin in the cell walls of Coccomyxa and Myrmecia phycobionts of various lichens: an ultrastructural and chemical investigation. Can. J. Bot. 59: 2713–2734.Google Scholar
  75. Hopkins J.A. and McCarthy F.M.G. 2002. Post-depositional palynomorph degradation in Quaternary shelf sediments: a laboratory experiment studying the effects of progressive oxidation. Palynology 26: 167–184.Google Scholar
  76. Hull H.M., Hoshaw R.W. and Wang J.-C. 1985. Interpretation of zygospore wall structure and taxonomy of Spirogyra and Sirogonium (Zygnemataceae, Chlorophyta). Phycologia 24: 231–239.Google Scholar
  77. Huss V.A.R., Frank C., Hartmann E.C., Hirmer M., Kloboucek A., Seidel B.M., Wenzeler P. and Kessler E. 1999. Biochemical taxonomy and molecular phylogeny of the genus Chlorella sensu lato (Chlorophyta). J. Phycol. 35: 587–598.Google Scholar
  78. Javaux E., Knoll A.H. and Walter M. 2003. Recognizing and interpreting the fossils of early eukaryotes. Origin. Life Evol. Biosph. 33: 75–94.Google Scholar
  79. Kadouri A., Derenne S., Largeau C., Casadevall E. and Berkaloff C. 1988. Resistant biopolymer in the outer walls of Botryococcus braunii, B race. Phytochemistry 27: 551–557.Google Scholar
  80. Kjellström G. 1968. Remarks on the chemistry and ultrastructure of the cell wall of some Palaeozoic leiospheres. Geol. Föreningens Stockholm Förhandl. 90: 221–228.Google Scholar
  81. Knoll A.H. 1992. The early evolution of eukaryotes: a geological perspective. Science 256: 622–627.PubMedGoogle Scholar
  82. Knoll A.H. 1996. Archean and Proterozoic paleontology. In: Jansonius J. and McGregor D.C. (eds.), Palynology: Principles and Applications, AASP Foundation, Salt Lake City, pp. 51–80.Google Scholar
  83. Kokinos J.P., Eglinton T.I., Goñi M.A., Boon J.J., Martoglio P.A. and Anderson D.M. 1998. Characterisation of a highly resistant biomacromolecular material in the cell wall of a marine dinoflagellate resting cyst. Org. Geochem. 28: 265–288.Google Scholar
  84. Kolattukudy P.E. 1981. Structure, biosynthesis and biodegradation of cutin and suberin. Ann. Rev. Plant Physiol 32: 539–576.Google Scholar
  85. König J. and Peveling E. 1980. Vorkommen von sporopollenin in der zellwand des phycobionten Trebouxia. Z. Pflanzenphysiol. 98: 459–464.Google Scholar
  86. König J. and Peveling E. 1984. Cell walls of the phycobionts Trebouxia and Pseudotrebouxia: constituents and their localisation. Lichenology 16: 129–144.Google Scholar
  87. Kozubek A. and Tyman J.H.P. 1999. Resorcinolic lipids, the natural non-isoprenic amphiphiles and their biological activity. Chem. Rev. 99: 1–26.PubMedGoogle Scholar
  88. Kuypers M.M.M., Blokker P., Hopmans E.C., Kinkel H., Pancost R.D., Schouten S. and Sinninghe Damsté J.S. 2002. Archaeal remains dominate marine organic matter from the early Albian oceanic anoxic event 1b. Palaeogeogr. Palaeoclimatol. Palaeoecol. 185: 211–234.Google Scholar
  89. Leppig U. and Montenari M. 2000. Organic-walled microfossils of possible dinoflagellate affinity from the Lower Permian of Sonora (northwest Mexico). Mar. Micropaleontol. 40: 1–8.Google Scholar
  90. Lewis J., Harris A.S.D., Jones K.J. and Edmonds R.L. 1999. Long-term survival of marine planktonic diatoms and dinoflagellates in stored sediment samples. J. Plankton Res. 21: 343–354.Google Scholar
  91. Lille Ü. 2003. Current knowledge on the origin and structure of Estonian Kukersite kerogen. Oil Shale 20: 253–263.Google Scholar
  92. Marchant H.J. 1977. Cell division and colony formation in the green alga Coelastrum (Chlorococcales). J. Phycol. 13: 102–110.Google Scholar
  93. Marret F. 1993. Les effets de l’acétolyse sur les assemblages des kystes de dinoflagelle’s. Palynoscience 2: 267–272.Google Scholar
  94. McKinney D.E., Bortiatynski J.M., Carson D.M., Clifford D.J., de Leeuw J.W. and Hatcher P.G. 1996. Tetramethylammonium hydroxide (TMAH) thermochemolysis of the aliphatic biopolymer cutan: insights into the chemical structure. Org. Geochem. 24: 641–650.Google Scholar
  95. Metzger P. and Largeau C. 1994. A new type of ether lipid comprising phenolic moieties in Botryococcus braunii. Chemical structure and abundance, and geochemical implications. Org. Geochem. 22: 801–814.Google Scholar
  96. Metzger P. and Largeau C. 2002. Natural polyacetals. In: Matsumura S. and Steinbüchel A. (eds.), Miscellaneous Biopolymers and Biodegradation of Synthetic Polymers, Wiley-VCH, Weinheim, pp. 113–127.Google Scholar
  97. Moldowan J.M., Dahl J., Jacobson S.R., Huizinga B.J., Fago F.J., Shetty R., Watt D.S. and Peters K.E. 1996. Chemostratigraphic reconstruction of biofacies: molecular evidence linking cyst-forming dinoflagellates with pre-Triassic ancestors. Geology 24: 159–162.Google Scholar
  98. Montsant A., Zarka A. and Boussiba S. 2001. Presence of a nonhydrolysable biopolymer in the cell wall of vegetative cells and astaxanthin-rich cysts of Haematococcus pluvialis (Chlorophyceae). Mar. Biotechnol. 3: 515–521.PubMedGoogle Scholar
  99. Morrill L.C. and Loeblich A.R. III 1981. The dinoflagellate pellicular wall layer and its occurrence in the division Pyrrophyta. J. Phycol. 17: 315–323.Google Scholar
  100. van Mourik A. 2000. Chemical characterization of fossil palynomorphs; gonyaulacoid, peridinioid dinoflagellate cysts and sporomorphs. Masters Thesis Department of Geochemistry, Utrecht University, 49 pp.Google Scholar
  101. Mösle B., Finch P., Collinson M.E. and Scott A.C. 1997. Comparison of modern and fossil plant cuticles by selective chemical extraction monitored by flash pyrolysis-gas chromatography-mass spectroscopy and electron microscopy. J. Anal. Appl. Pyrolysis 40–41: 585–597.Google Scholar
  102. Mulder M.M., van der Hage E.R.E. and Boon J.J. 1992. Analytical in source pyrolytic methylation electron impact mass spectrometry of phenolic acids in biological matrices. Phytochem. Anal. 3: 165–172.Google Scholar
  103. Müller P.J., Kirst G., Ruhland G., Von Storch I. and Rosell-Melé A. 1998. Calibration of the alkenone paleotemperature index based on coretops from the eastern South Atlantic and global ocean (60°N-60°S). Geochim. Cosmochim. Acta 62: 1757–1772.Google Scholar
  104. Porcella R.A. and Walne P.L. 1980. Microarchitecture and envelope development in Dysmorphococcus globosus (Phacotaceae, Chlorophyceae). J. Phycol. 16: 280–290.Google Scholar
  105. Puel F., Largeau C. and Giraud G. 1987. Occurrence of a resistant biopolymer in the outer walls of the parasitic alga Prototheca wickerhamii (Chlorococcales): ultrastructure and chemical studies. J. Phycol. 23: 649–656.Google Scholar
  106. Rascio N., Casadoro G. and Andreoli C. 1979. Ultrastructural features of Chlorella nana sp. nov. Bot. Mar. 22: 223–227.Google Scholar
  107. Rodríguez M.C. and Cerezo A.S. 1996. The resistant ‘biopolymer’ in cell walls of Coelastrum sphaericum. Phytochemistry 43: 731–734.Google Scholar
  108. Rodríguez M.C., Noseda M.D. and Cerezo A.S. 1999. The fibrillar polysaccharides and their linkage to algaenan in the trilaminar layer of the cell wall of Coelastrum sphaericum (Chlorophyceae). J. Phycol. 35: 1025–1031.Google Scholar
  109. Rozema J., Broekman R.A., Blokker P., Meijkamp B.B., de Bakker N., van de Staaij J., van Beem A., Ariese F. and Kars S.M. 2001. UV-B absorbance and UV-B absorbing compounds (para-cumaric acid) in pollen and sporopollenin: the perspective to track historic UV-B levels. J. Photochem. Photobiol. 62: 108–117.Google Scholar
  110. Rozema J., van Geel B., Björn L.O., Lean J. and Madronich S. 2002. Toward solving the UV puzzle. Science 296: 1621–1622.PubMedGoogle Scholar
  111. Rullkötter J. 1993. The thermal alteration of kerogen and the formation of oil. In: Engel M.H. and Macko S.A. (eds.), Organic Geochemistry. Principles and Applications, Plenum Press, New York, pp. 377–96.Google Scholar
  112. Sarjeant W.A. 1978. Arpylorus antiquus Calandra, emend., a dinoflagellate cyst from the Upper Silurian. Palynol. 2: 167–179.Google Scholar
  113. Schenck P.A., de Leeuw J.W., van Graas G., Haverkamp J. and Bouman M. 1981. Analysis of recent spores and pollen and of thermally altered sporopollenin by flash pyrolysis-mass spectrometry and flash pyrolysis-gas chromatography-mass spectrometry. In: Brooks J. (ed.) Organic Maturation Studies and Fossil Fuel Exploration, Academic Press, London, pp. 225–237.Google Scholar
  114. Schouten S., Hopmans E.C., Schefuss E. and Sinninghe Damsté J.S. 2002. Distributional variations in marine crenarchaeotal membrane lipids: a new tool for reconstructing ancient sea water temperatures? Earth Planet. Sci. Lett. 204: 265–274.Google Scholar
  115. Schrank E. 1988. Effects of chemical processing on the preservation of peridinioid dinoflagellates: a case from the late cretaceous of NE Africa. Rev. Palaeobot. Palynol. 56: 123–140.Google Scholar
  116. Shaw G. 1971. The chemistry of sporopollenin. In: Brooks J. (ed.), Sporopollenin, Academic Press, London, pp. 305–350.Google Scholar
  117. Simpson A.J., Zang X., Kramer R. and Hatcher P.G. 2003. New insights on the structure of algaenan from Botryococcus braunii race A and its hexane insoluble botryals based on multidimensional NMR spectroscopy and electrospray-mass spectrometry techniques. Phytochem. 62: 783–796.Google Scholar
  118. Sinninghe Damsté J.S., Delas Heras F.X.C., de Bergen P.F. and de Leeuw J.W. 1993. Characterization of tertiary catalan lacustrine oil shales: discovery of extremely organic sulphurrich Type I kerogens. Geochim. Cosmochim. Acta 57: 389–415.Google Scholar
  119. Srivastava A. and Prasad R. 2000. Triglycerides-based diesel fuels. Renew. Sust. Energ. Rev. 4: 111–133.Google Scholar
  120. Staehelin L.A. and Picket-Heaps J.D. 1975. The ultrastructure of Scenedesmus (Chlorophyceae). I. Species with the ‘reticulate’ or ‘warty’ type of ornamental layer. J. Phycol. 11: 163–185.Google Scholar
  121. Stankiewicz B.A., Briggs D.E.G., Michels R., Collinson M.E., Flannery M.B. and Evershed R.P. 2000. Alternative origin of aliphatic polymer kerogen. Geology 28: 559–562.Google Scholar
  122. Strother P.K. 1996. Acritarchs. In: Jansonius J. and McGregor D.C. (eds.), Palynology: principles and applications, AASP Foundation, Salt Lake City, pp. 81–106.Google Scholar
  123. Swift E. and Remsen C.C. 1970. The cell wall of Pyrocystis spp. (Dinophyceae). J. Phycol. 6: 79–86.Google Scholar
  124. Syrett P.J. and Thomas E.M. 1973. The assay of nitrate reductase in whole cells of Chlorella: strain differences and the effect of cell walls. New Phytol. 72: 1307–1310.Google Scholar
  125. Talyzina N.M., Moldowan J.M., Johannisson A. and Fago F.J. 2000. Affinities of Early Cambrian acritarchs studied by using microscopy, fluorescence flow cytometry and biomarkers. Rev. Palaeobot. Palynol. 108: 37–53.Google Scholar
  126. Tegelaar E.W., de Leeuw J.W., Derenne S. and Largeau C. 1989. A reappraisal of kerogen formation. Geochim. Cosmochim. Acta 53: 3103–3106.Google Scholar
  127. Tegelaar E.W., Kerp H., Visscher H., Schenck P.A. and de Leeuw J.W. 1991. Bias of the paleobotanical record as a consequence of variations in the chemical composition of higher vascular plant cuticles. Paleobiology 17: 133–144.Google Scholar
  128. Tiffany L.H. 1924. A physiological study of growth and reproduction among certain algae. Ohio J. Sci. 24: 65–99.Google Scholar
  129. Turon J.-L. 1984. Le palynoplancton dans l’environnement actuel de l’Atlantique nord-oriental. Évolution climatique et hydrologique depuis le dernier maximum glaciaire. Mem. Inst. Geol. Bassin Aquitaine 17: 1–313.Google Scholar
  130. Versteegh G.J.M., Blokker P., Wood G., Collinson M.E., Sinninghe Damsté J.S. and de Leeuw J.W. 2004. Oxidative polymerization of unsaturated fatty acids as a preservation pathway for microalgal organic matter. Org. Geochem. 35: 1129–1139.Google Scholar
  131. Versteegh G.J.M., Jansen J.H.F., de Leeuw J.W. and Schneider R.R. 2000. Mid-chain diols and keto-ols in sediments. A new tool for tracing past sea surface water masses?. Geochim. Cosmochim. Acta 64: 1879–1892.Google Scholar
  132. Versteegh G.J.M. and Zonneveld K.A.F. 2002. Use of selective degradation to separate preservation from productivity. Geology 30: 615–618.Google Scholar
  133. Warnaar J. 2001. Chemical characterization of fossil organic walled dinoflagellate cysts. Masters Thesis, Department of Geochemistry, Utrecht University. 26 pp.Google Scholar
  134. Wehling K., Niester C., Boon J.J., Willemse M.T.M. and Wiermann R. 1989. p-Coumaric acid — a monomer in the sporopollenin skeleton. Planta 179: 376–380.Google Scholar
  135. Wicander R., Foster C.B. and Reed J.D. 1996. Green and bluegreen algae. Gloeocapsomorpha. In: Jansonius J. and McGregor D.C. (eds.), Palynology: Principles and Applications, AASP Foundation, Salt Lake City, pp. 215–225.Google Scholar
  136. Wurdack M.E. 1923. Chemical composition of the walls of certain algae. Ohio J. Sci. 23: 181–191.Google Scholar
  137. Yule B.L., Roberts S. and Marchall J.E.A. 2000. The thermal evolution of sporopollenin. Org. Geochem. 31: 859–870.Google Scholar
  138. Zárský V., Kalina T. and Sulek J. 1985. Notes on the sexual reproduction of Chlamydomonas geitleri Ettl. Arch. Protistenk. 130: 343–353.Google Scholar
  139. Zelibor J.L. Jr, Romankiw L., Hatcher P.G. and Colwell R.R. 1988. Comparitive analysis of the chemical composition of mixed and pure cultures of green algae and their decomposed residues by 13C nuclear magnetic resonance spectroscopy. Appl. Env. Microbiol. 54: 1051–1060.Google Scholar
  140. Zhang E., Hatcher P.G. and Davis A. 1993. Chemical composition of pseudo-phlobaphinite precursors: implications for the presence of aliphatic biopolymers in vitrinite from coal. Org. Geochem. 20: 721–734.Google Scholar
  141. Zonneveld K.A.F., Versteegh G.J.M., and de Lange G. J. 1997. Preservation of organic walled dinoflagellate cysts in different oxygen regimes: a 10,000 years natural experiment. Mar. Micropaleontol. 29: 393–405.Google Scholar
  142. Zonneveld K.A.F., Versteegh G.J.M. and de Lange G.J. 2001. Palaeoproductivity and post-depositional aerobic organic matter decay reflected by dinoflagellate cyst assemblages of the Eastern Mediterranean S1 sapropel. Mar. Geol. 172: 181–195.Google Scholar

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© Springer 2005

Authors and Affiliations

  1. 1.Royal Netherlands Institute for Sea ResearchTexelThe Netherlands
  2. 2.Organic Geochemistry, Faculty of GeosciencesUtrecht UniversityUtrechtThe Netherlands
  3. 3.Faculty of BiologyPalaeoecologyUtrechtThe Netherlands
  4. 4.Hanse WissenschaftskollegDelmenhorstGermany
  5. 5.Shell Global Solutions InternationalAmsterdamThe Netherlands

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