Characterization of a highly resistant biomacromolecular material in the cell wall of a marine dinoflagellate resting cyst

Organic Geochemistry

Volumn 28, Issue 5, 1998, Pages 265-288

  Kokinos, John P ^a,d   Eglinton, Timothy I ^a   Goñi, Miguel A ^a,e   Boon, Jaap J ^b   Martoglio, Pamela A ^c,f   Anderson, Donald M ^a  

^a WOODS HOLE OCEANOGRAPHIC INSTITUTION   (United States)

^b FOM INSTITUTE AMOLF   (Netherlands)

^c Building 8   (United States)

^d Hellenic College Holy Cross   (United States)

^e UNIVERSITY OF SOUTH CAROLINA   (United States)

^f Nicholet Instrument Corp   (United States)

Author keywords

Algaenans; Biomacromolecules; Dinoflagellates; Resting cysts; Sporopollenin

Indexed keywords

ALGAE; FOURIER TRANSFORM INFRARED SPECTROSCOPY; GAS CHROMATOGRAPHY; HYDROLYSIS; MACROMOLECULES; MASS SPECTROMETRY; PROTOZOA; PYROLYSIS; SAPONIFICATION; SOLVENT EXTRACTION;

ACID HYDROLYSIS; BIOMACROMOLECULES; CELL WALL; CURIE POINT PYROLYSIS; CYST; DINOFLAGELLATE; ELEMENTAL ANALYSIS; LIGHT MICROSCOPY; LINGULODINIUM POLYEDRUM; SPOROPOLLENIN;

ANALYTICAL GEOCHEMISTRY;

GONYAULAX POLYEDRA; LINGULODINIUM POLYEDRUM;

EID: 0032540208     PISSN: 01466380     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0146-6380(97)00134-4     Document Type: Article

References (97)

1. Allard, B., Templier, J. and Largeau, C. (1997) Artifactual origin of mycobacterial bacteran. Formation of melanoidin-like artifactual macromolecular material during the usual isolation process. Org. Geochem. 21, in press.
2. 14C acetate, studied in synchronous cultures Planta. 107:1972;1-32.
3. Barss M. S., Williams G. L. Palynology and nannofossil processing techniques. Geol. Surv. Can. Pap. 73(26):1973;1-25.
4. Berkaloff C., Casadevall E., Largeau C., Metzger P., Peracca S., Virlet J. The resistant polymer of the walls of the hydrocarbon-rich alga Botryococcus braunii. Phytochemistry. 22:1983;389-397.
5. Bibby B. T., Dodge J. D. The encystment of a freshwater dinoflagellate: a light and electron microscopical study. Br. Phycol. J. 7:1972;85-100.
6. Boon J. J. Analytical pyrolysis mass spectroscopy: new vistas opened by temperature-resolved in-source PYMS. Int. J. Mass Spectrom. Ion Process. 118/119:1992;755-787.
7. Brunner U., Honegger R. Chemical and ultrastructural studies on the distribution of sporopolleninlike biopolymers in six genera of lichen phycobionts. Can. J. Bot. 63:1985;2221-2230.
8. Bujak, J. P. and Davies, E. H. (1983) Modern and Fossil Peridiniineae. AASP Contribution Series Number 13, 203 p. American Association of Stratigraphic Palynologists Foundation.
9. Burczyk J. Biogenetic relationships between ketocarotenoids and sporopollenins in green algae. Phytochemistry. 26:1987;113-119.
10. Burczyk J. Cell wall carotenoids in green algae which form sporopollenins. Phytochemistry. 26:1987;121-128.
11. Burczyk J., Dworzanski J. Comparison of sporopollenin-like algal resistant polymer from cell wall of Botryococcus. Scenedesmus and Lycopodium clavatum by GC-pyrolysis. Phytochemistry. 27:1988;2151-2153.
12. Burton G. W., Ingold K. U. Vitamin E: Application of the principles of physical organic chemistry to the exploration of its structure and function. Acc. Chem. Res. 19:1986;194-201.
13. Chaloner, W. G. and Orbell, G. (1971) A palaeobiological definition of sporopollenin. In Sporopollenin, ed. J. Brooks, P. R. Grant, M. Muir, P. van Gijzel and G. Shaw, p. 273-294. Proceedings of a symposium held at the Geology Department, Imperial College, London, 23-25 September, 1970, Academic Press, London.
14. Correia, M. (1971) Diagenesis of sporopollenin and other comparable organic substances: Application to hydrocarbon research. In Sporopollenin, ed. J. Brooks, P. R. Grant, M. Muir, P. van Gijzel and G. Shaw, p. 569-620. Proceedings of a symposium held at the Geology Department, Imperial College, London, 23-25 September, 1970, Academic Press, London.
15. Cowie G. L., Hedges J. I., Prahl F. G., de Lange G. J. Elemental and major biochemical changes across an oxidation front in a relict turbidite: An oxygen effect. Geochim. Cosmochim. Acta. 59:1995;33-46.
16. de Leeuw, J. W. and Largeau, C. (1993) A review of macromolecular organic compounds that comprise living organisms and their role in kerogen, coal, and petroleum formation. In Organic Geochemistry, ed. M. H. Engel and S. A. Macko, pp. 23-72. Plenum Press, New York.
17. de Leeuw, J. W., Baas, M., Brinkhuis, H., and Sinninghe Damsté, J. S. (1993). Cyst cell wall biomacromolecules and dinosterol derivatives: molecular fossils of dinoflagellates. 5th International Conference on Modern and Fossil Dinoflagellates, Zeist, the Netherlands, April 18-24, 1993, Abstract, pp. 28-29.
18. Delwiche C. F., Graham L. E., Thomson N. Lignin-like compounds and sporopollenin in Coleochaete, an algal model for land plant ancestry. Science. 245:1989;399-401.
19. Derenne S., Largeau C., Casadevall E., Berkaloff C. Occurrence of a resistant biopolymer in the L race of Botryococcus braunii. Phytochemistry. 28:1989;1137-1142.
20. Derenne S., Largeau C., Casadevall E., Sellier N. Direct relationship between the resistant biopolymer and the tetraterpenic hydrocarbon in the lycopadiene race of Botryococcus braunii. Phytochemistry. 29:1990;2187-2192.
21. Derenne S., Largeau C., Casadevall E., Berkaloff C., Rousseau B. 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. 55:1991;1041-1050.
22. Derenne S., Largeau C., Berkaloff C., Rousseau B., Wilhelm C., Hatcher P. G. Non-hydrolysable macromolecular constituents from outer walls of Chlorella fusca and Nanochlorum eucaryotum. Phytochemistry. 31:1992;1923-1929.
23. Derenne S., Largeau C., Berkaloff C. First example of an algaenan yielding an aromatic-rich pyrolysate. Possible geochemical implications on marine kerogen formation. Org. Geochem. 24:1996;617-627.
24. de Vries P. J. R., Simons J., van Beem A. P. Sporopollenin in the spore wall of Spirogyra (Zygnemataceae Chlorophyceae). Acta Bot. Neerl. 32:1983;25-28.
25. Douglas A. G., Sinninghe Damste J. S., Fowler M. G., Eglinton T. I., de Leeuw J. W. Unique distributions of hydrocarbons and sulfur compounds released by flash pyrolysis from the fossilised alga Gloeocapsomorpha prisca, a major constituent in one of four Ordovician kerogens. Geochimica Cosmochimica Acta. 55:1991;275-291.
26. Eglinton T. I., Boon J. J., Minor E. C., Olson R. J. Microscale characterization of algal and related particulate organic matter by direct temperature-resolved mass spectrometry. Mar. Chem. 52:1996;27-54.
27. Eisenack A. Hystrichosphären. Bio. Rev. Cambridge Philos. Soc. 38:1963;107-139.
28. Erdtman G. The acetolysis method. A revised description. Sven. Bot. Tidskr. 54:1961;561-564.
29. Evitt W. R. Observations on the morphology of fossil dinoflagellates. Micropaleontology. 7:1961;385-420.
30. Evitt, W. R. (1985) Sporopollenin Dinoflagellate Cysts: Their Morphology and Interpretation, 333 p. American Association of Stratigraphic Palynologists Foundation.
31. Fensome, R. A., Taylor, F. J. R., Norris, G., Sarjeant, W. A. S., Wharton, D. I. and Williams, G. L. (1993) A Classification of Living and Fossil Dinoflagellates. Micropaleontology, Special Publication Number 7, 351 p. Sheridan Press, Hanover, PA.
32. Flaviano C., Le Berre F., Derenne S., Largeau C., Connan J. First indications of the formation of kerogen amorphous fractions by selective preservation. Role of non-hydrolysable macromolecular constituents of Eubacterial cell walls. Org. Geochem. 22:1994;759-771.
33. Fritz L., Anderson D. M., Triemer R. E. Ultrastructural aspects of sexual reproduction in the red tide dinoflagellate Gonyaulax tamarensis. J. Phycol. 25:1989;95-107.
34. Gelin F., Boogers I., Noordeloos A. A. M., Hatcher P. G., Sinninghe Damste J. S., de Leeuw J. W. Novel, resistant microalgal polyethers: An important sink of organic carbon in marine environments? Geochim. Cosmochim. Acta. 60:1996;1275-1280.
35. Geisert M., Rose T., Bauer W., Zahn R. K. Occurrence of carotenoids and sporopollenin in Nanochlorum eucaryotum a novel marine alga with unusual characteristics. BioSystems. 20:1987;133-142.
36. ñi and Hedges, 1990a.
37. Goñi M. A., Hedges J. I. Cutin-derived CuO reaction products from purified cuticles and tree leaves. Geochim. Cosmochim. Acta. 54:1990;3065-3072.
38. ñi and Hedges, 1990b.
39. Goñi M. A., Hedges J. I. The diagenetic behavior of cutin acids in buried conifer needles and sediments from a coastal marine environment. Geochim. Cosmochim. Acta. 54:1990;3083-3093.
40. ñi and Hedges, 1992.
41. Goñi M. A., Hedges J. I. Lignin dimers: Structures, distribution, and potential geochemical applications. Geochim. Cosmochim. Acta. 56:1992;4025-4043.
42. ñi and Hedges, 1993.
43. Goñi M. A., Hedges J. I. Molecular-level characterization of marine-derived sedimentary organic matter by alkaline CuO oxidation: sources and reactivities of organic matter from Skan Bay (Alaska) sediments. Chem. Geol. 107:1993;483-485.
44. ñi et al., 1993.
45. Goñi M. A., Nelson B., Blanchette R. A., Hedges J. I. Fungal degradation of wood lignins: Geochemical perspectives from CuO-derived phenolic dimers and monomers. Geochim. Cosmochim. Acta. 57:1993;3985-4002.
46. ñi et al., 1995.
47. Goñi, M. A., Kokinos, J. P., Hatcher, P. and Eglinton, T. I. (1995) Chemical, pyrolytic and spectroscopic characterization of resistant biopolymer(s) present in pollen. In Organic Geochemistry: Developments and Applications to Energy, Climate, Environment and Human History, ed. J. O. Grimalt and C. Dorronsoro, pp. 983-985. Selected papers from the 17th International Meeting on Organic Geochemistry, 4th-8th September 1995, Donostia-San Sebastián, The Basque Country, Spain, A.I.G.O.A.
48. ñi et al., 1998.
49. Goñi, M. A., Kokinos, J. P., Hatcher, P., Boon, J. J., Martoglio, A. and Eglinton, T. I. (1998) Chemical, pyrolytic and spectroscopic characterization of resistant biopolymers present in pollen, in preparation.
50. Good B. H., Chapman R. L. The ultrastructure of Phycopeltis (Chroolepidaceae: Chlorophyta). I. Sporopollenin in the cell walls. Am. J. Bot. 65:1978;27-33.
51. Goodman D. K. (1987) Dinoflagellate cysts in ancient and modern sediments. In The Biology of Dinoflagellates, ed. F. J. R. Taylor, Vol. 21, pp. 649-722. Botanical Monographs, Blackwell Scientific Publishers, Oxford.
52. Goossens H., de Leeuw J. W., Schenck P. A., Brassell S. C. Tocopherols as likely precursors of pristane in ancient sediments and crude oils. Nature. 312:1984;440-442.
53. Goth K., de Leeuw J. W., Püttmann W., Tegelaar E. W. Origin of messel oil shale kerogen. Nature. 339:1988;759-761.
54. Gray, J. (1965) Techniques in palynology; Part III. In Handbook of Paleontological Techniques, ed. B. Kummel and D. M. Raup, pp. 469-706. Freeman and Company, San Francisco.
55. 13C NMR spectroscopy of sporopollenins from different plant taxa Plant Physiol. 86:1988;134-136.
56. Hedges J. I., Ertel J. R. Characterization of lignin by capillary gas chromatography of cupric oxide oxidation products. Anal. Chem. 54:1982;174-178.
57. Herminghaus S., Gubatz S., Arendt S., Wiermann R. The occurrence of phenols as degradation products of natural sporopollenin - a comparison with "synthetic sporopollenin" Z. Naturforsch. 43c:1988;491-500.
58. Jux U. Über den feinbau der wandungen einiger Tertiärer dinophyceen-zysten und achritarcha Hystichosphaeridium, Impletosphaeridium, Lingulodinium. Palaeontographica, Abt. B. 132:1971;165-174.
59. Kadouri A., Derenne S., Largeau C., Casadevall E., Berkaloff C. Resistant biopolymer in the outer walls of Botryococcus braunii, B race. Phytochemistry. 27:1988;551-557.
60. Keil R. G., Hu F. S., Tsamakis E., Hedges J. I. Pollen grains deposited in marine sediments are degraded only under oxic conditions. Nature. 369:1994;639-641.
61. Kokinos, J. P. (1994) Studies on the cell wall of dinoflagellate resting cysts: Morphological development, ultrastructure, and chemical composition. Ph. D. Thesis, Massachusetts Institute of Technology/Woods Hole Oceanographic Institution, Technical Report WHOI-94-10, 234 p.
62. Kokinos J. P., Anderson D. M. Morphological development of resting cysts in cultures of the marine dinoflagellate Lingulodinium polyedrum (=L. machaerophorum). Palynology. 19:1995;143-166.
63. önig and Peveling, 1980.
64. König J., Peveling E. Vorkommen von sporopollenin in der zellwand des phycobionten Trebouxia. (Sporopollenin in the cell wall of the phycobiont Trebouxia). Z. Pflanzenphysiol. (Int. J. Plant Physiol.). 98:1980;459-464.
65. Largeau C., Casadevall E., Kadouri A., Metzger P. Formation of Botryococcus-derived kerogens - Comparative study of immature torbanites and of the extant alga Botryococcus braunii. Org. Geochem. 6:1984;327-332.
66. Largeau C., Derenne S., Casadevall E., Kadouri A., Sellier N. Pyrolysis of immature Torbanite and of the resistant biopolymer (PRB A) isolated from the extant alga Botryococcus braunii. Mechanism of formation and structure of Torbanite. Org. Geochem. 10:1986;1023-1032.
67. Larter S. R., Solli H., Douglas A. G., De Lange F., de Leeuw J. W. The occurrence and significance of prist-1-ene in kerogen pyrolysates. Nature. 279:1979;405-408.
68. Larter, S. R., Solli, H. and Douglas, A. G. (1981) Phytol-containing melanoidins and their bearing on the fate of isoprenoid structures in sediments. In Advances in Organic Geochemistry, ed. M. Bjorøy et al.), pp. 513-523. Proceedings of the 10th International Meeting on Organic Geochemistry, University of Bergen, Norway, 14-18 September 1981.
69. Larter, S. R. and Horsfield, B. (1993) Determination of structural components of kerogens by the use of analytical pyrolysis methods. In Organic Geochemistry, ed. M. H. Engel and S. A. Macko, pp. 271-287. Plenum Press, New York.
70. Li M., Larter S. R., Taylor P., Jones D. M., Bowler B., Bjorøy M. Biomarkers or not biomarkers? A new hypothesis for the origin of pristane involving derivation from methyltrimethyltridecylchromans (MTTCs) formed during diagenesis from chlorophyll and alkylphenols. Org. Geochem. 23:1995;159-167.
71. Morrill L. C., Loeblich A. R. III The dinoflagellate pellicular wall layer and its occurrence in the division Pyrrhophyta. J. Phycol. 17:1981;315-323.
72. Mulder M. M., van der Hage E. R. E., Boon J. J. Analytical in source pyrolytic methylation electron impact mass spectrometry of phenolic acids in biological matrices. Phytochem. Anal. 3:1992;165-172.
73. Pfiester, L. A. (1984) Sexual reproduction. In Dinoflagellates, ed. D. L. Spector, pp. 181-199. Academic Press, Orlando, FL.
74. Pfiester L. A. Dinoflagellate sexuality. Int. Rev. Cytol. 114:1989;249-272.
75. Pfiester, L. A. and Anderson, D. M. (1987) Dinoflagellate Reproduction. In The Biology of Dinoflagellates, ed. F. J. R. Taylor, Vol. 21, pp. 611-648. Botanical Monographs, Blackwell Scientific Publishers, Oxford.
76. Prahl A. K., Springstubbe H., Grumbach K., Wiermann R. Studies on sporopollenin biosynthesis: The effect of inhibitors of carotenoid biosynthesis on sporopollenin accumulation. Z. Naturforsch. 40c:1985;621-626.
77. Puel F., Largeau C., Giraud G. Occurrence of a resistant biopolymer in the outer walls of the parasitic alga Prototheca wickerhamii (Chlorococcales): Ultrastructure and chemical studies. J. Phycol. 23:1987;649-656.
78. Rouxhet, P. G., Robin, P. L. and Nicaise, G. (1980) Characterization of kerogens and of their evolution by infrared spectroscopy. In Kerogen: Insoluble Organic Matter from Sedimentary Rocks, ed. B. Durand, pp. 163-190. Éditions Technip, Paris.
79. Sarjeant W. A. S. Review of Evitt, W. R., 1985, Sporopollenin Dinoflagellate Cysts: Their Morphology and Interpretation. Micropaleontology. 32:1986;282-285.
80. Schmitter R. E. The fine structure of Gonyaulax polyedra, a bioluminescent marine dinoflagellate. J. Cell Sci. 9:1971;147-173.
81. Schmitter R. E. (1989) Structure and function of globular bodies in dinoflagellate cells [Abstract]. Fourth International Conference on Modern and Fossil Dinoflagellates, p. 92, Marine Biological Laboratory, Woods Hole, Massachusetts, Program and Abstracts.
82. Schultze Osthoff K., Weirmann R. Phenols as integrated compounds of sporopollenin from Pinus pollen. J. Plant Physiol. 131:1987;5-15.
83. Shaw G., Yeadon A. Chemical studies on the constitution of some pollen and spore membranes. J. Chem. Soc. C. 1:1966;16-22.
84. Spector, D. L. (Ed.) (1984) Dinoflagellates, 545 p., Academic Press, Orlando, FL.
85. Tappan, H. (1980) The Paleobiology of Plant Protists, 1028 p. W. H. Freeman and Company, San Francisco.
86. Taylor D. L. In situ studies on the cytochemistry and ultrastructure of a symbiotic marine dinoflagellate. J. Mar. Biol. Assoc. U.K. 48:1968;349-366.
87. Taylor, F. J. R. (Ed.) (1987) The Biology of Dinoflagellates. Botanical Monographs, Vol. 21, 785 p. Blackwell Scientific Publications, Oxford.
88. Tegelaar E. W., de Leeuw J. W., Derenne S., Largeau C. A reappraisal of kerogen formation. Geochim. Cosmochim. Acta. 53:1989;3103-3106.
89. Tegelaar, E. W. (1990) Resistant biomacromolecules in morphologically characterized constituents of kerogen: A key to the relationship between biomass and fossil fuels. Ph.D. thesis, Rijksuniversiteit Utrecht.
90. van Bergen P. F., Collinson M. E., Sinninghe Damsté J. S., de Leeuw J. W. Chemical and microscopical characterization of inner seed coats of fossil water plants. Geochim. Cosmochim. Acta. 58:1994;231-239.
91. van Bergen P. F., Goñi M., Collinson M. E., Barrie P. J., Sinninghe Damsté J. S., de Leeuw J. W. Chemical and microscopic characterization of outer seed coats of fossil and extant water plants. Geochim. Cosmochim. Acta. 58:1994;3823-3844.
92. Walker, L. M. (1984) Life histories, dispersal, and survival in marine, planktonic dinoflagellates. In Marine Plankton Life Cycle Strategies, ed. K. A. Steidinger and L. M. Walker, p. 19-34. CRC Press, Boca Raton, FL.
93. Wehling K., Niester C., Boon J. J., Willemse M. T. M., Wiermann R. p-Coumaric acid - a monomer in the sporopollenin skeleton. Planta. 179:1989;376-380.
94. Williams, G. L. and Bujak, J. P. (1985) Mesozoic and Cenozoic dinoflagellates. In Plankton Stratigraphy, ed. H. M. Bolli, J. B. Saunders and K. Perch-Nielsen, pp. 847-964. Cambridge Earth Science Series, Cambridge University Press, Cambridge.
95. Williams G. L., Stover L. E., Kidson E. J. Morphology and stratigraphic ranges of selected Mesozoic-Cenozoic dinoflagellate taxa in the northern hemisphere. Geol. Surv. Can. Pap. 92(10):1993;1-137.
96. Zetsche F., Kalt P., Leichti J., Ziegler E. Zur konstitution des lycopodiumsporinins des tasmins und des lange-sporonins. J. Prakt. Chem. 148:1937;67-84.
97. Zetsche F., Vicari H. Untersuchungen über die membran der sporen und pollen. Helv. Chim. Acta. 14:1931;58-78.