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    Studies on the cell wall of dinoflagellate resting cysts : morphological development, ultrastructure, and chemical composition

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    Date
    1994-06
    Author
    Kokinos, John P.  Concept link
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    Citable URI
    https://hdl.handle.net/1912/5565
    DOI
    10.1575/1912/5565
    Keyword
     Palynology; Dinoflagellates; Encystment 
    Abstract
    This thesis presents a series of investigations on the specialized cell covering of a dormant stage (the resting cyst) in the life cycle of the marine dinoflagellate Lingulodinium polyedra. These cell walls, along with those of resting cysts formed by many other dinoflagellate species, are resistant to degradation and persist in the depositional environment. Selective preservation of these materials has created a rich dinoflagellate fossil record (extending back ~225 million years) which has shown great utility in biostratigraphic applications. By elucidating the nature of resting cyst walls and directly observing their development in laboratory cultures, the research presented here addresses several long-standing questions regarding both the paleontology and biology of dinoflagellates. Although resting cyst formation has been reported in other extant species, this thesis documents for the first time the morphological development of resting cysts having "fossilizable", morphologically complex cell walls. In laboratory cultures of L. polyedra, resting cyst formation is an extremely rapid phenomenon; the transition from thecate, actively swimming planozygote to spine-bearing, morphologically mature hypnozygote occurs within 10-20 minutes. The basic mechanism consists of dramatic cell expansion resulting from the widening of an interstice between the planozygotic cytoplasm and a balloon-like membrane external to the theca. Key morphological events in the development of the distinctive L. polyedra resting cyst cell covering occur within this interstice. These include early dissociation and outward migration of the theca, formation of the resistant endophragm, and growth of spines from globules on the surface of the cytoplasm. The level of morphological maturity attained by the encysting cell depends primarily on how much development occurs before rupture of the expanding outer membrane. H rupture is premature, a wide variation of resting cyst morphology may occur, particularly with respect to the size, number, and distribution of processes. The direct observation of these developmental events has shed much light on several issues regarding resting cyst morphogenesis. First, growth of L. polyedra resting cyst spines is clearly centrifugal (i.e. growing radially outward). Although not necessarily representative of spine growth in all species, this mode of formation provides a useful preliminary framework for interpreting some of the "histrichosphaerid" morphologies present in the fossil record. Second, in this species at least, the theca plays no direct role in influencing the morphology of spines. Finally, considerable variation in spine morphology is possible within one biologically-defined species. This last point has considerable significance for cyst-based taxonomy, and strongly suggests that several of the fossil morphotypes traditionally designated as separate species of Lingulodinium are, in fact, synonymous. Ultrastructural examination of L. polyedra resting cysts formed in laboratory culture has shown, for the first time, the fine structure of the cell walls enclosing a living, paleontologically-signillcant resting cyst. Unfortunately, difficulties associated with fixation and infiltration of these thick-walled structures precluded an in-depth investigation of the ultrastructural dynamics underlying the morphological development described above. Preliminary results, however, confirm earlier speculation that only the outermost wall of the L. polyedra resting cyst is normally preserved in the fossil record. This outer wall (including spines) appears constructed of closely appressed structural units, an ultrastructural style apparently widespread among species related to L. polyedra. The resistant cell walls of L. polyedra resting cysts were isolated from laboratory cultures and chemically characterized by an extensive array of analytical techniques. Both thermal (pyrolysis) and chemical (CuO oxidation) dissociation of this material yielded suites of products consistent with a macromolecular substance composed signillcantly of aromatic components. In addition, the relative abundance of carboxylated phenols among resting cyst CuO oxidation products indicated that aromatic structural units in the dinoflagellate material may be largely carbon-carbon linked, probably directly through aromatic nuclei. Such a "condensed" arrangement may be, in part, responsible for the remarkable resistance of the dinoflagellate resting cyst wall biopolymer. Overall, the aromatic signature of L. polyedra resting cyst wall material can be clearly distinguished from that of both pollen wall "sporopollenin" and classical lignin. Although some short chain carboxylic acids are generated during CuO oxidation, there is little evidence obtained by dissociation techniques to suggest the significant presence of extended polymethylenic elements in this macromolecular substance. As a result, the dinoflagellate material appears fundamentally different from the highly aliphatic "algaenans" recently identified in the cell wall of several chlorophyte species. Interestingly, pyrolysis (Py-GC/MS) of resting cyst wall material produced an abundance ofprist-1-ene, strongly suggesting the presence of bound tocopherols which may play an important structural role in the resistant cell wall biopolymer. Lipid analysis of L. polyedra culture extract revealed a series of even carbon numbered fatty acids (C14 - C24), as well as sterols (including dinosterol and cholesterol), and a full suite of tocopherols. These compounds are present during construction of the resistant outer wall of the resting cyst, and could function as precursors to the resting cyst wall biopolymer. Another possibility, given the strong aromaticity predicted by the results of pyrolysis and CuO oxidation, is some contribution by aromatic amino acids in an analogous fashion to lignin biosynthesis. The extensive chemical characterization of the outermost cell wall of L. polyedra resting cysts reported in this thesis provides the first rigorous analysis of "fossilizable" biopolymer(s) produced by an extant dinoflagellate. Furthermore, these analyses represent an unprecedented level of chemical characterization of a resistant algal cell wall biopolymer, and clearly demonstrate the unique nature of the L. polyedra resting cyst wall. As a result, this work provides the first chemical data to justify the term "dinosporin", previously proposed to distinguish the highly resistant material comprising dinoflagellate resting cyst walls from other resistant cell wall biopolymers.
    Description
    Submitted in partial fulfillment of the requirements for the degree of Doctor of Philosophy at the Massachusetts Institute of Technology and the Woods Hole Oceanographic Institution June 1994
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    • Biology
    • WHOI Theses
    Suggested Citation
    Thesis: Kokinos, John P., "Studies on the cell wall of dinoflagellate resting cysts : morphological development, ultrastructure, and chemical composition", 1994-06, DOI:10.1575/1912/5565, https://hdl.handle.net/1912/5565
     

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