MICROBIOLOGICAL REVIEWS, Dec. 1992, p. 529-542 Vol. 56, No. 4 0146-0749/92/040529-14$02.00/0 Copyright © 1992, American Society for Microbiology Relationship between the Flagellates and the Ciliates ROBERT EDWARD LEE'* AND PAUL KUGRENS2 Department ofAnatomy and Neurobiologyl* and Department ofBiology, 2 Colorado State University, Fort Collins, Colorado 80523 INTRODUCTION ....................................................................... 529 COMPARISONS BASED ON MORPHOLOGICAL AND CYTOLOGICAL STRUCTURES .................529 Dinoflagellates and Ciliates ....................................................................... 529 Comparison of dinoflagellates and ciliates ....................................................................... 531 (i) Cortical alveoli ....................................................................... 531 (ii) Mitochondrial cristae ........................................................................ 531 (iii) Structures of cilia, flagella, and associated structures .....................................................532 (a) Grouping and number of cilia and flagela....................................................................532 (b) Surface and subsurface of cilia and flagela ........................................ ...................532 (c) Basal body structure ....................................................................... 533 (d) Type of ciliaryn ecklace .......................................................................533 (e) Type of ciliary and flagelar roots ....................................................................... 533 (I) Summary of similarities in cilia and flageUla of the ciliates and dinoflagellates .......................533 (iv) Parasomal sac and pusule ....................................................................... 533 (v) Extrusive organelles ........................................................................ 533 (vi) Feeding apparatus ....................................................................... 534 (vii) Nucleus ....................................................................... 535 Summary of the similarities between dinoflagellates and ciliates ................................................535 Comparison of Colponema loxodes and Ciliates ........................................................................ 535 Similarity between Suctorian Ciliates and the Flagellate Katablepharis ...........................................535 Characteristics of Katablepharis spp........................................................................535 Characteristics of suctorian ciliates ....................................................................... 535 Comparison of suctorian ciliates and Katablephars spp ...........................................................536 COMPARISONS BASED ON MOLECULAR STRUCTURE ..........................................................537 rRNA Nucleotide Sequencing .......................................................................538 Use of mRNA Codons ....................................................................... 538 CONCLUSION ....................................................................................... 539 INTRODUCTION dence, for the close relationship between the ciliates and the flagellates. The ciliates have long been recognized as a distinct group of organisms (26, 79, 114). The following classical features distinguish the ciliates from other organisms. (i) They exhibit COMPARISONS BASED ON MORPHOLOGICAL AND nuclear dualism (the possession of two types of nuclei). They CYTOLOGICAL STRUCTURES have a germ line diploid micronucleus, which is transcrip- The dinoflagellates and two genera of uncertain taxonomic tionally inactive, and a vegetative polyploid macronucleus, position, Colponema and Katablepharis, are the flagellates which is responsible for transcription in the cell. (ii) They with morphological and cytological structures most similar possess cilia at some stage in their life history. Each cilium to those of the ciliates. A comparison of each of these with has a kinetosome (basal body) with characteristic fibrillar the ciliates is presented. structures in the cytoplasm associated with it. (iii) They have alveoli in the cortical cytoplasm. An alveolus consists of a Dinoflagellates and Ciliates single flattened membrane cistemum that usually occurs beneath the plasma membrane and commonly has rows of Historically, the dinoflagellates have generally been con- microtubules under it. There are ciliates that lack one or sidered to be the most likely ancestors of the ciliates. In the more of the above characteristics. However, the vast major- 1800s, it was thought that the beating waves of the trans- ity of ciliates have these three features. verse flagellum encircling the cell in the cingulum of di- The flagellates have been considered to be the closest noflagellates was actually produced by the waves of closely relatives of the ciliates, with their unicellular nature and the packed cilia (23, 27, 68). This observation resulted in the similarity in the structure of cilia and flagella providing the inclusion of the dinoflagellates in the phylum Cilioflagellata basis of this relationship (20, 22, 27, 80, 113, 115, 120, 121). with the ciliates. In the following review, we will present first the morpholog- More recently, Taylor (120, 121, 122) (Fig. 1) presented a ical and cytological evidence, and then the molecular evi- phylogenetic tree with the ciliates arising from a branch just above the dinoflagellates. The resemblance between the cortical structures of the ciliates and dinoflagellates was * Corresponding author. presented as the strongest argument for the closeness of the 529 530 LEE AND KUGRENS MICROBIOL. REV. TUBULAR CRISTAE IN TAYLOR MITOCHONDRIA Oomycetes ,'Hyphochytrids ' FLATTENED CRISTAE !N MITOCHONDRIA / : SMALL AND LYNN Bodonids ! , Euglenoids TTrypanosomes ', Chromophyte Cryptophytes Choanoflagellates, Postciliodesmata .... Charophytes Algae Rhabdophora Cyrtophora Chiorophytes Chytrids Prasinophytes * #,l0.... Ciliates Dinophytes8 Zygomycetes . - ---"'''%\ Basidiomycete$ Colponema i oRhodophytes..yt.Ascomycetes Dinoflagellates8- Corticoflagellate Animals CAVALIER-SMITH Fungi. CRYPTISTA CHROMOBIOTA PLANTS (Cryptophytes)aN(Chromophytelgae) Two membranes of endoplasmic Chlrllstbnlalchloroplasttubular CILIOPHORACiiCiliaLOpHrAepresent(ieites(Ciliates) reticulum,flagellar hairs DINOZOA (Dinoflagellates) Cortical alveoli (OxyrrhiCHOANOZOA OPALOZOA Tubular mitochondrial cristae, no cortical alveoli no tubular flagellar hairs (Heteromita) PARABASALIA EUGLENOZOA (Euglenoids) Hydrogenosomes as respiratory Two flagella, specialized Z.- . organelles instead of feeding apparatus (Bodo) mitochondria (Trichomonas) PERCOLOZA Commonly with four flagella, discoid mitochondrial cristae, peroxisomes (Percolomonas, Naegleria, Tetramitus, Stephanopogon) t M ETAMONADA Four flagella, non-amoeboid, no mitochondria, no peroxisome, no dictyosomes (Hexamita) ARCHAMOEBAE Uniflagellate amoebae, no mitochondria, no peroxisome, no dictyosomes (Mastigamoeba) FIG. 1. Portions of evolutionary schemes that have involved the relationship between the dinoflagellates and the ciliates. two groups. Other authors have derived the ciliates from the by mitosis followed by only partial cytokinesis. Such a dinoflagellates through the dinoflagellate Polykrikos sp. (20, multiplication of the nuclei and flagella within a single cell 92, 113). Polykrikos sp. is a multinucleate and multiflagellate has been considered a first step toward the multinucleate and dinoflagellate that consists basically of a number of di- multiciliated condition in the ciliates. noflagellate cells stacked one on top of another and fused to Cavalier-Smith also believed that the ciliates evolved from produce a single cell. This dinoflagellate probably evolved the dinoflagellates (20-22) (Fig. 1) and placed both in the VOL. 56, 1992 FLAGELLATE-CILIATE RELATIONSHIP 531 Posterior Anterior FIG. 2. Structure of a cell of a typical ciliate. subphylum Corticoflagellata. The Corticoflagellata is char- (i) Cortical alveoli. The cortical alveoli in the ciliates are acterized by a highly developed cortical microtubular sys- flattened membrane sacs that lie just beneath the plasma tem, a phagocytic mode of nutrition, a strong tendency to membrane and above the epiplasm (Fig. 2; see also Fig. 4) evolve repeated cortical structures and multiple nuclei, (26, 79, 115). A row of microtubules frequently occurs genomes or cells, and the absence of the transitional region beneath the alveoli. The dinoflagellates have flattened thecal star and of tubular mastigonemes. Similarly, Small and Lynn vesicles under the plasma membrane (Fig. 3 and 4) (31, 32) (78, 115) (Fig. 1) derived the ciliates from a corticoflagellate that appear to be similar to the cortical alveoli of the ciliates. ancestor, with the dinoflagellates arising from a branch In the dinoflagellates, the thecal vesicles are commonly filled immediately under the ciliates. Corliss (24, 27) has reviewed with thecal plates. Like the cortical alveoli of the ciliates, the the relationship of the ciliates with the flagellates and has thecal vesicles often lie above a row of microtubules. Cav- also come to the conclusion that the dinoflagellates represent alier-Smith (22) argues that the thecal vesicles are an evolu- the most probable ancestor of the ciliates. tionary response to predation, with the thecal plates acting Comparison of dinoflagellates and ciliates. The dinoflagel-