Dinoflagellate Life-Cycle Complexities
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J. Phycol. 38, 417–419 (2002) DINOFLAGELLATE LIFE-CYCLE COMPLEXITIES The dinoflagellates are a group of predominately pseudopodial network illustrated by Hofender (1930) marine, alveolate protists whose structural organiza- as an anastomosing feeding structure of Ceratium hi- tion, morphological diversity, and novel behaviors have rundinella is likely an artifact of cell trauma, while the captured the imaginations of phycologists and proto- juxtaposition of a small Protoperidinium within the sul- zoologists for 250 years. The 2000 or so extant species cus of Ceratium lunula, interpreted by Norris (1969) as that comprise the dinoflagellates sort almost equally evidence of feeding, may represent spurious, post- as phototrophs and heterotrophs; however, a growing mortem placement of specimens (Jacobson 1999). awareness that many species are really mixotrophic, Successful cultivation of dinoflagellates was not engaging in some combination of phototrophy and achieved until early in the twentieth century when phagotrophy, is eroding the conventional view of di- Crypthecodinium cohii was first grown on rotting pieces noflagellate nutrition (Stoecker 1999). The intricate of the brown algae Fucus (Taylor 1987). Since then, jigsaw puzzles formed by the thecal plates of armored only a small percentage of dinoflagellate species have species (Fensome et al. 1993, Steidinger and Tangen been successfully brought into culture. Most of these 1996), the complex light-sensing organelles of the War- are neritic, photosynthetic species whose growth re- nowiacids (Gaines and Elbrächter 1987), and unique quirements are tolerant of high cell densities typically feeding structures, including zipper-like “mouths” for achieved in culture. Oceanic forms seem more diffi- swallowing food, peduncles or feeding tubes for “suck- cult to grow, perhaps due to their intolerance of con- ing-up” whole prey or their cytoplasmic contents, and taminants associated with culture glassware (Loeblich feeding veils for encasing and externally digesting 1984), while heterotrophic dinoflagellates often re- large prey (Jacobson and Anderson 1986, Buck et al. quire the availability of appropriate prey or host spe- 1990, Hansen and Calado 1999), are but a few of the cies. Not surprisingly, therefore, early studies of di- remarkable features that make dinoflagellates truly noflagellate autecology were based on observations of exceptional. Equally fascinating are the colors exhib- living or preserved field samples and were thus lim- ited by dinoflagellates, ranging from the opalescent ited by availability of suitable material and the occur- blues, greens, and pinks of heterotrophic forms to yel- rence of ephemeral life-history stages. Linking pre- lows, reds, and browns of photosynthetic species (Ko- sumed life-history stages in the absence of cultures foid and Swezy 1921, Lebour 1925). This amazing ar- often requires assumptions that can lead to inaccurate ray of pigmentations led Kofoid and Swezy (1921) to life cycles and taxonomic confusion. The case of Pyro- comment that dinoflagellates “. are most brilliantly cystis lunula and Dissodinium pseudolunula is a good ex- colored, vying with orchids and butterflies in variety ample. The taxonomic history of these genera is long of color and delicacy of shading.” and varied, dating back to the early observations of The study of dinoflagellates, however, has not been Murray during the voyage of the Challenger Expedi- without its drawbacks. Difficulties encountered when tion (see Elbrächter and Drebes 1978 for details). For examining delicate, sometimes rare specimens are almost a century, life-history stages of P. lunula and D. not only frustrating, but can lead to misinterpretation pseudolunula were mistakenly aggregated into a single and erroneous conclusions. Changes in temperature incomplete life cycle. Only after cultures were estab- and osmotic stress associated with desiccation during lished (Swift and Durbin 1971; Drebes 1978) was it microscopic examination can cause cellular distor- possible to demonstrate the existence of two species, tion, ecdysis, or loss of integrity. Many dinoflagellates, one free-living and one parasitic, and to complete particularly athecate species, are notoriously difficult their life cycles and reveal that the two organisms be- to preserve, with chemical fixatives producing mis- longed to separate orders (Elbrächter and Drebes shapen cells, swollen membranes, and clumping of 1978; Drebes 1978). specimens. Such phenomena may account for some The availability of cultures has also proved impor- of the unusual reports that have failed to be corrobo- tant in demonstrating the relevance of sexuality and rated by subsequent investigators. For example, the encystment in the life cycles and ecology of dino- 417 418 ALGAE • HIGHLIGHTS flagellates (Walker 1984 and references therein). Ex- thors sequenced the small subunit ribosomal RNA cept for Noctiluca, all dinoflagellates examined thus gene and confirmed that it matched sequence data far have haplontic life cycles dominated by asexual re- previously published for P. piscicida (Litaker et al. production of haploid vegetative cells (Pfiester and 1999, Oldach et al. 2000). Life-cycle processes were Anderson 1987). Temporary or pellicle cysts formed examined for cultures fed algal prey (Rhodomonas sp.) in response to adverse environmental conditions and and for cultures grown in the presence of fish (40–80 division cysts produced following feeding or growth mm goldfish or tilapia). Conventional light micros- are known to occur within the asexual cycle of several copy, video microscopy, fluorescent nuclear stains, species (von Stosch 1973, Dale 1983, Drebes and and electron microscopy were eloquently combined Schnepf 1988, Skovgaard 1996). A sexual phase has to determine the morphology and nuclear comple- also been documented for many dinoflagellates and ment of life-history stages and to document morpho- involves the fusion of asexually generated gametes to genetic events associated with stage transformations. produce a motile zygote, the planozygote. Planozy- The work required development of a new protocol to gotes may undergo meiosis to reestablish the haploid permeablize cysts for application of nuclear fluoro- phase, or produce a resting cyst (the hypnozygote), chromes. Results demonstrate that the life cycle of P. with cells reentering the asexual cycle upon germina- piscicida is haplontic, including asexual and sexual tion. Polymorphism is pronounced in some dino- phases that resemble patterns previously reported for flagellates, particularly the parasitic species (Cachon other dinoflagellates. Furthermore, life-cycle events were and Cachon 1987), and can result in rather elaborate the same whether cultures were grown on alga prey or life histories. Among the more remarkable dinoflagel- in the presence of fish. The life cycle of P. piscicida as late life cycles are those reported for members of the described by Litaker et al. (2002) differs greatly from Phytodiniales. For example, Cystodinedria inermis appears prior reports (Burkholder and Glasgow 1995, 1997). to have some 35 life-history stages encompassing bi- It has relatively few life-history stages, lacks amoeboid flagellate cells, a variety of lobose and filose amoeboid forms, and does not include spiny, chrysophyte-like forms, and encysted stages (Pfiester and Popovský cysts. 1979, Popovský and Pfiester 1982). Unfortunately, the Litaker et al. (2002) never observed amoeboid life cycle of C. inermis is known only from field collec- forms or flagellate-amoeba transitions in Pfiesteria pis- tions and should be viewed with caution. This is of cicida cultures grown on algal prey. They did, how- particular concern as some stages in the life cycle of ever, recover amoebae from cultures grown in the C. inermis are believed to be identical to Actinophrys sol presence of fish and from fish tanks that contained and other protists that are well documented in the lit- P. piscicida. Amoebae from both sources resembled erature as distinct and valid species (Popovský and amoeboid stages previously reported as part of the life Pfiester 1982). cycle of P. piscicida (Burkholder and Glasgow 1995, The toxic dinoflagellate Pfiesteria piscicida Steidinger 1997). To test the hypothesis that these amoebae were et Burkholder (Steidinger et al. 1996) also has a life-history stages of P. piscicida, Litaker et al. (2002) highly complex life cycle, with the 24 or more life-his- developed a suite of fluorescently labeled peptide nu- tory stages including a number of flagellated cell cleic acid probes for use in in situ hybridization stud- types, smooth walled and spiny, chrysophyte-like cysts, ies. A probe specific for the SSU rRNA of P. piscicida and amoebae with filose and lobose pseudopods failed to react with amoebae associated with P. pisci- (Burkholder and Glasgow 1995, 1997). Stages differ cida and fish, while a group-specific probe for the SSU greatly in size ranging from Ͻ10 m flagellates to 400 rRNA of the amoebae failed to react with P. piscicida. m amoebae. Some of the amoeboid forms are appar- The authors thus concluded that amoebae present in ently identical to species of planktonic and benthic their cultures were not part of the life cycle of P. pisci- amoebae described by earlier researchers (Burk- cida. holder and Glasgow 1997). While P. piscicida can be Results of studies like that of Litaker et al. (2002) maintained in culture with algal prey, induction of are always constrained by the number of