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Oogamous Reproduction, with Two-Step Auxosporulation, in the Centric Diatom Thalassiosira Punctigera (Bacillariophyta)1

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Oogamous Reproduction, with Two-Step Auxosporulation, in the Centric Diatom Thalassiosira Punctigera (Bacillariophyta)1 J. Phycol. 42, 845–858 (2006) r 2006 by the Phycological Society of America DOI: 10.1111/j.1529-8817.2006.00244.x OOGAMOUS REPRODUCTION, WITH TWO-STEP AUXOSPORULATION, IN THE CENTRIC DIATOM THALASSIOSIRA PUNCTIGERA (BACILLARIOPHYTA)1 Victor A. Chepurnov Laboratory of Protistology and Aquatic Ecology, Department of Biology, Ghent University, Krijgslaan 281 S8, 9000 Gent, Belgium David G. Mann Royal Botanic Garden, Edinburgh EH3 5LR, Scotland, UK Peter von Dassow, E. Virginia Armbrust Marine Molecular Biotechnology Laboratory, School of Oceanography, Box 357940, University of Washington, Seattle, Washington 98195, USA Koen Sabbe, Renaat Dasseville and Wim Vyverman2 Laboratory of Protistology and Aquatic Ecology, Department of Biology, Ghent University, Krijgslaan 281 S8, 9000 Gent, Belgium Thalassiosira species are common components of Key index words: auxosporulation; centric dia- marine planktonic communities worldwide and are toms; inbreeding; life cycle; mating; oogamy; sex- used intensively as model experimental organisms. ual reproduction; Thalassiosira However, data on life cycles and sexuality within Abbreviations: DAPI, 4,6-diamidino-2-phenylindole the genus are fragmentary. A clone of the cosmo- politan marine diatom Thalassiosira punctigera Cleve emend. Hasle was isolated from the North Sea and oogamous sexual reproduction was ob- Thalassiosira Cleve emend. Hasle is a large genus of served in culture. Cells approximately 45 lm and centric diatoms containing over 100 species, mainly smaller became sexualized. Oogonia were produced from marine and brackish habitats (Hasle and Syvert- preferentially and spermatogenesis was infrequent. sen 1996). Thalassiosira species are very common in Unfertilized oogonia always aborted and their de- planktonic communities worldwide and some are used velopment was apparently arrested at prophase of intensively in experimental studies of cell physiology meiosis I. Further progression through meiosis and and biochemistry (Peers and Price 2004, Zhukova auxospore formation occurred only after a sperm 2004), including advanced methods of molecular ge- had penetrated into the oocyte. Many cells of the netics (Armbrust 1999, 2000, Armbrust and Galindo new large-celled generation (approximately 90– 2001). Cell wall formation has been studied in detail in 120 lm in size) immediately became sexualized Thalassiosira eccentrica (Ehrenb.) Cleve (Schmid and again but only oogonia were produced. A few of Schulz 1979, Schmid 1984a, b) and recently the first the large oogonia became auxospores and produced whole diatom genome was sequenced in T. pseudonana initial cells 132–153 lm in diameter. The second Hasle and Heimdal (Armbrust et al. 2004). step of auxosporulation probably involved fertiliza- Isolating new cultures and providing conditions tion of large-celled oocytes by the sperm of the that favor vegetative multiplication are generally not small-celled spermatogonangia that were still pre- problematic in diatoms, but there are often difficulties in the long-term maintenance of clones (von Stosch sent in the culture. An F1 clone obtained after self- ing within the small-celled auxosporulation size 1965, Chepurnov et al. 2004, Mann and Chepurnov range was investigated. Like the parent clone, the 2004). The main problem is that most diatoms studied exhibit a gradual cell size reduction during vegetative F1 clone was homothallic but no auxosporulation was observed: spermatogonangia were unable to cell division, according to the principle known as the produce viable sperm, apparently because of in- MacDonald–Pfitzer rule (Crawford 1981, Pickett- breeding depression. Aggregation and interaction Heaps et al. 1990). There is overwhelming experimen- of oogonia were documented, and may be relevant tal evidence that, due to size reduction, cells sooner or for understanding the mechanisms of signaling and later become critically small and die in cultures that recognition between sexualized cells and the evolu- exhibit purely vegetative growth (Geitler 1932, Rosh- tion of sexuality in pennate diatoms. chin 1994, Mann et al. 1999, Chepurnov et al. 2004). The principal mechanism of cell size restitution is through formation of specialized cells called auxo- 1Received 21 December 2005. Accepted 25 April 2006. spores. These quickly expand in volume (hours, less 2Author for correspondence: e-mail [email protected]. often days) and afterwards a new large cell (the initial 845 846 VICTOR A. CHEPURNOV ET AL. cell) is formed inside the auxospore envelope; the in- ual reproduction in the auxospore mother cell. We itial cell can then resume vegetative multiplication. have confirmed the accuracy of these reports in isolates Each auxospore typically results from a sexual repro- of the same species collected from different parts of the duction event and represents the cell formed after fu- world with those from which the original reports were sion of two haploid gametes: it is essentially a special made during the course of studies for Ha˚kansson and type of zygote, although the gametic nuclei often re- Chepurnov (1999) and Chepurnov et al. (2004). All of main unfused during the early stages of auxospore the clones isolated behaved identically, in that au- development (Round et al. 1990). Exceptions in which xosporulation was completed successfully without any auxosporulation is asexual, or where size is restored signs of spermatogenesis. Spermatogenesis did occur via a morphogenetically different process called vege- at other times, but normally appeared only in small tative cell enlargement, seem to be rare (Chepurnov cells and, as reported previously (Erben 1959, Schultz et al. 2004). Thus, sexuality and auxosporulation are and Trainor 1968, Drebes 1977a), fertilization of au- central to understanding diatom cell size reduction– xospore mother cells by sperm was never seen. Nagai restitution life cycles, with profound consequences for et al. (1995) found simultaneous auxosporulation and interpretations of population dynamics in nature. spermatogenesis in multiple strains of the planktonic Very little is yet known about the biochemical and marine centric diatom Coscinodiscus wailesii Gran. They genetic mechanisms underpinning the sexual behavior did not exclude the possibility that oogamous sexual of diatoms. The first information on cell cycle regula- reproduction might occur in natural populations of tion of diatom sexuality was obtained from a Thalassios- this diatom but in culture, auxospores developed ex- ira species, T. weissflogii (Grun.) Fryxell and Hasle. Cells clusively by asexual processes and again fertilization by of T. weissflogii are sensitive to induction of spermato- sperm did not occur. Finally, in several clones of Act- genesis in the early G1 phase of the cell cycle (Armb- inoptychus senarius (Ehrenberg) Ehrenberg [syn. A. un- rust et al. 1990) and molecular studies (Armbrust dulatus (Bailey) Ralfs], meiosis was circumvented in 1999, 2000) have revealed a novel gene family (the most of the cells predetermined to become oogonia Sig-genes) that is suggested to be specific to sexual re- and these cells developed into auxospores partheno- production. The SIG polypeptides may play a role in genetically (Behre and von Stosch in Drebes 1977a). sperm–egg recognition and could therefore be poten- Thus, the formation of sperm and auxospores within a tial molecular markers for sexual reproduction in nat- culture does not prove that oogamy occurs; direct ob- ural populations of centric diatoms (Armbrust 1999). servation of fertilization is needed. The DNA sequences of Sig1 genes have since been ob- We selected T. punctigera (Castracane) Hasle for tained for three more Thalassiosira species (T. oceanica study because it is large-celled, morphologically dis- Hasle, T. guillardii Hasle, and T. pseudonana), and some tinctive, and very common worldwide in marine coast- geographically distant isolates of T. weissflogii (Armb- al plankton (Hasle 1983), where it sometimes produces rust and Galindo 2001). blooms (Horner 2002). Additionally, T. punctigera Despite the importance of Thalassiosira species as grows well in culture and has already been used as models for studying aspects of diatom sexuality, there an experimental organism representative of the dia- is a surprising absence of basic information concerning toms as a whole (Hamm et al. 2003, Vrieling et al. gametogenesis, fertilization, and auxospore formation, 2005). Although T. punctigera has already been shown which have been documented in some detail in only to auxosporulate in monoclonal cultures (Hasle and two Thalassiosira species, namely T. eccentrica (Drebes Syvertsen 1996, p. 49, Fig. 12), details of this process 1979, Schmid 1984a) and T. lacustris (Grunow) Hasle have not been documented. We demonstrate sexual (Idei 1993). In T. weissflogii, abundant evidence of vig- reproduction in T. punctigera, providing a basis for us- orous induction of spermatogenesis has been provided ing this species for studies of the genetic and physio- in experimental cultures (Vaulot and Chisholm 1987, logical control of sexuality in centric diatoms. Armbrust et al. 1990, Armbrust 1999). However, no evidence has yet been provided on the occurrence of oogenesis and auxospores in this species, either in cul- MATERIALS AND METHODS ture or in nature. Unfortunately, spermatogenesis and A planktonic sample containing T. punctigera cells was col- reports of periodic increases and decreases in mean lected on May 24, 2002 in the Westerschelde (Zeeland, the 1 0 1 0 cell size in cultures
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