American Journal of Botany 91 10 1523 1534 2004 DINOFLAGELLATES A REMARKABLE EVOLUTIONARY EXPERIMENT1 JEREMIAH D HACKETT 2 DONALD M ANDERSON 3 DEANA L ERDNER 3 AND DEBASHISH BHATTACHARYA2 4 Department of Biological Sciences and Center for Comparative Genomics University of Iowa Iowa City Iowa 52242 USA and 3 Biology Department Woods Hole Oceanographic Institution Woods Hole Massachusetts 02543 USA 2 In this paper we focus on dinoflagellate ecology toxin production fossil record and a molecular phylogenetic analysis of hosts and plastids Of ecological interest are the swimming and feeding behavior bioluminescence and symbioses of dinoflagellates with corals The many varieties of dinoflagellate toxins their biological effects and current knowledge of their origin are discussed Knowledge of dinoflagellate evolution is aided by a rich fossil record that can be used to document their emergence and diversification However recent biogeochemical studies indicate that dinoflagellates may be much older than previously believed A remarkable feature of dinoflagellates is their unique genome structure and gene regulation The nuclear genomes of these algae are of enormous size lack nucleosomes and have permanently condensed chromosomes This chapter reviews the current knowledge of gene regulation and transcription in dinoflagellates with regard to the unique aspects of the nuclear genome Previous work shows the plastid genome of typical dinoflagellates to have been reduced to single gene minicircles that encode only a small number of proteins Recent studies have demonstrated that the majority of the plastid genome has been transferred to the nucleus which makes the dinoflagellates the only eukaryotes to encode the majority of typical plastid genes in the nucleus The evolution of the dinoflagellate plastid and the implications of these results for understanding organellar genome evolution are discussed Key words dinoflagellate endosymbiosis evolution harmful algal blooms The dinoflagellates division Pyrrhophyta class Dinophyceae are an important group of phytoplankton in marine and fresh waters Their adaptation to a wide variety of environments is reflected by a tremendous diversity in form and nutrition and an extensive fossil record dating back several hundred million years Graham and Wilcox 2000 As swimming cells they can flourish under conditions that are unsuitable for many nonmotile phytoplankton a success due in part to unique behavior patterns including diel vertical migration migration through the water column on a 24 h cycle Some dinoflagellates produce toxins that are dangerous to man marine mammals fish seabirds and other components of the marine food chain Van Dolah 2000 Others are bioluminescent and emit light some function as parasites or symbionts that rely on host organisms for part of their nutrition Many dinoflagellates are photosynthetic and through endosymbiosis have acquired a wide diversity of plastids from distant evolutionary lineages The most common plastid in dinoflagellates has been subject to drastic evolutionary changes that we are only beginning to understand An equal number of dinoflagellates obtain their carbon by ingesting other phytoplankton Many are now being shown to have both of these traits i e to be mixotrophic It is thus no surprise that these organisms have been extensively studied and classified as plants by some workers and as animals by others General characteristics Whether living as a swimming solitary cell or a nonmotile symbiont within an invertebrate host all living dinoflagellates have certain common characteristics Steidinger 1983 Most photosynthetic species contain chlorophylls a and c2 the carotenoid beta carotene and a group of xanthophylls that appears to be unique to dinoflagellates typically peridinin dinoxanthin and diadinoxanthin 1 4 Manuscript received 20 January 2004 revision accepted 4 June 2004 Author for reprint requests These pigments give many dinoflagellates their typical goldenbrown color However some dinoflagellates have acquired other pigments through endosymbiosis including fucoxanthin see the following plastid discussion Two different cell types can be distinguished on the basis of the cell wall covering or theca The naked or unarmored forms have an outer plasmalemma surrounding a single layer of flattened vesicles These cells are fragile and distort easily Armored dinoflagellates have cellulose or other polysaccharides within each vesicle giving the cells a more rigid inflexible wall These cellulose plates are arranged in distinct patterns called tabulation which are extensively used as taxonomic fingerprints For a detailed discussion of dinoflagellate taxonomy see Fensome et al 1993 The dinoflagellate nucleus is unique in several ways as elaborated in more detail later The chromosomes for example are easily visible at all stages of growth because they do not go through coiling and uncoiling as is common in other phytoplankton but instead remain permanently condensed Dinoflagellates also have few or no nucleosomes associated with their DNA and a unique pattern of mitosis Spector 1984 Because these characteristics are so different from both eukaryotic and prokaryotic cells a new intermediate kingdom Mesokaryota was once proposed for them Dodge 1965 Yet another distinguishing characteristic of dinoflagellates is that their motile cells have two unequal flagella One is a flattened ribbon like flagellum which encircles the cell in a transverse groove providing propulsive and spinning force for the cell The other flagellum is directed posteriorly along a longitudinal groove and presumably acts like a rudder for steering Although all dinoflagellates share certain physiological and structural characteristics they exhibit a tremendous diversity in external morphology Some cells are small and smoothly spherical whereas others have elaborate structures that resemble horns wings collars or even arms and hands with fingers 1523 1524 AMERICAN JOURNAL OF BOTANY Vol 91 Ecology Several aspects of the behavior physiology and ecology of dinoflagellates are notable and will be highlighted next These include swimming behavior bioluminescence heterotrophy symbiosis and toxicity Swimming behavior As motile cells dinoflagellates are capable of directed swimming behavior in response to a variety of parameters These include chemotaxis phototaxis and geotaxis for which movement is controlled by chemical stimuli light or gravity respectively It
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