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Life Cycle, Size Reduction Patterns, and Ultrastructure of the Pennate Planktonic Diatom Pseudo-Nitzschia Delicatissima (Bacillariophyceae)1

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Life Cycle, Size Reduction Patterns, and Ultrastructure of the Pennate Planktonic Diatom Pseudo-Nitzschia Delicatissima (Bacillariophyceae)1 View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by Lirias J. Phycol. 41, 542–556 (2005) r 2005 Phycological Society of America DOI: 10.1111/j.1529-8817.2005.00080.x LIFE CYCLE, SIZE REDUCTION PATTERNS, AND ULTRASTRUCTURE OF THE PENNATE PLANKTONIC DIATOM PSEUDO-NITZSCHIA DELICATISSIMA (BACILLARIOPHYCEAE)1 Alberto Amato, Luisa Orsini,3 Domenico D’Alelio, and Marina Montresor2 Stazione Zoologica ‘‘A. Dohrn,’’ Villa Comunale, 80121 Naples, Italy Pseudo-nitzschia delicatissima (Cleve) Heiden is a Diatoms have complex life cycles, including a pecu- very common pennate planktonic diatom found in liar division mode and, in some, the capacity to pro- temperate marine waters, where it is often responsi- duce resting stages (Round et al. 1990, Edlund and ble for blooms. Recently, three distinct internal tran- Stoermer 1997). Because of the constraint represented scribed spacer types have been recorded during a by the rigid silica frustule that surrounds the cell, di- P. delicatissima bloom in the Gulf of Naples (Medi- atoms undergo progressive size reduction as vegetative terranean Sea, Italy), which suggests the existence of growth proceeds. Cell size is usually restored through cryptic diversity. We carried out mating experiments a sexual phase, which includes the formation of a with clonal strains belonging to the most abundant unique type of cell, the auxospore, that is not sur- internal transcribed spacer type. Pseudo-nitzschia deli- rounded by the siliceous frustule and is therefore catissima is heterothallic and produces two functional capable of expansion. Inside the auxospore, the anisogametes per gametangium. The elongated au- formation of a large-sized vegetative cell, called the in- xospore possesses a transverse and a longitudinal itial cell, takes place (Round et al. 1990, Mann 1993a). perizonium. The sexual phase was observed to occur The basic pattern of the sexual cycle differs between overawidesizespectrum,spanning19–80lmand centric and pennate diatoms. Centric diatoms evolved corresponding to almost the whole range of cell first (Kooistra et al. 2003) and are characterized by length observed for P. delicatissima.Wealsoinvesti- oogamous reproduction, involving the formation of gated cell morphology, valve ultrastructure and uniflagellate male gametes (sperms) and larger non- morphometry of parental, F1-generation strains, motile female gametes, whereas pennates produce and the progeny of crosses between parental and F1 nonmotile morphologically identical but sometimes be- strains. Although ultrastructural features match those haviorally different gametes (Round et al. 1990). With- described for P. delicatissima, variability in cell shape in these two major types, there are many variants was recorded in the largest cells of the F1 generation characterized by distinct morphological and behavi- as well as in valves with an abnormal arrangement of oral traits, which may be helpful in revealing evolu- poroids. As many other diatoms, P. delicatissima un- tionary relationships among taxa (von Stosch 1982, dergoes size reduction over its life cycle, and cells of Theriot 1992, Mann 1999). different size showed differences in growth rates and A critical link between diatom cell size and the onset the amount of size reduction per cell cycle. Cells be- of the sexual phase has been reported for several spe- tween 60 and 30 lminlengthshowedthefastest cies: Gametogenesis generally occurs within cells of the growth and the slowest rates of size reduction per smaller size classes, usually below 30%–40% of the di- generation. In culture, P. delicatissima cells can de- mensions of the maximum cell size (Round et al. crease to 8 lm in length; however, such small cells 1990). In addition, vegetative enlargement has been ( 30 lm) are not recorded in the sea, and this raises reported for a few diatoms, for example, the centric interesting questions about the factors that control diatoms Ditylum brightwellii (West) Grunow (von Stosch their survival in the natural environment. 1965), Leptocylindrus danicus Cleve (French and Har- Key index words: life cycle; morphology; Pseudo- graves 1985), and Skeletonema costatum (Greville) Cleve nitzschia delicatissima; sexual reproduction; size (Gallagher 1983) and the pennate diatom Achnanthes reduction (Chepurnov and Mann 1997). These species are able to regain a larger size while bypassing the sexual phase: Cells inflate, producing an auxospore-like structure, Abbreviations: ITS, internal transcribed spacer; L:D, and then build a new and larger pair of valves (von light:dark Stosch 1965, Gallagher 1983, Nagai et al. 1995). Life histories have important implications for dia- tom ecology. Undergoing a sexual phase is crucial for many diatom species to regain cells with a larger size. 1Received 7 July 2004. Accept 2 February 2005. 2Author for correspondence: e-mail [email protected]. Moreover, sex allows for genetic recombination, and 3Present address: University of Helsinki, P.O. Box 65 (Viikinkaari 1), the frequency of sexual events should have a funda- FIN-00014 Finland. mental role in shaping the genetic structure of diatom 542 LIFE CYCLE OF PSEUDO-NITZSCHIA DELICATISSIMA 543 populations. A variety of sexual strategies with differ- generation strains were established by the isolation of single ent levels of synchronization and triggering modes has initial cells and maintained as described above. been reported and correlated with ecological factors Mating experiments. Mating experiments between parental (McQuoid and Hobson 1996, Edlund and Stoermer strains were performed on different occasions during the progressive size reduction of the cultures. Before running 1997). However, life history patterns, including the the experiments, 30 cells of each strain were measured at sexual cycle, have been investigated for only a very 400Â magnification using an Axiophot light microscope limited number of species, if we consider the extreme (Carl Zeiss, Oberkochen, Germany) equipped with an ocular evolutionary, morphological, and ecological diversity micrometer. Cultures in exponential growth phase (approx- of this group of marine algae. Most studies have dealt imately 5 Â 104 cells Á mL–1) were used for testing mating with freshwater benthic species (Geitler 1979, Mann compatibility. Pairs of strains were inoculated together into tissue-culture plate wells filled with 5 mL of f/2 medium and 1993a, Mann et al. 2003), and relatively little informa- incubatedatatemperatureof201 C, a photon fluence rate of tion is available for marine planktonic diatoms (Edlund about 100 mmol photons Á m–2 Á s–1, and a 14:10-h L:D photo- and Stoermer 1997, Mann 1993b). cycle. Control wells were inoculated with double the volume We describe the life cycle of Pseudo-nitzschia del- (0.4mL) of each parental strain to test for the presence of icatissima (Cleve) Heiden, a chain-forming marine intraclonal sexual reproduction. Culture plates were inspect- pennate diatom, with a wide distribution range in ed daily with a Zeiss Axiovert inverted microscope to check for the presence of sexual stages. The different life stages both oceanic and coastal waters (Hasle 2002). Species were observed and measured via a Zeiss Axiovert and/or identification within the genus Pseudo-nitzschia is often Axiophot microscope and photographed using a Zeiss Axio- troublesome and requires the examination of fine cam digital system. The presence and arrangement of the ultrastructural characters of the silica frustule in chloroplasts in the auxospores were observed with the Zeiss TEM (Hasle and Syvertsen 1997). A recent study car- Axiophot microscope using the Zeiss epifluorescence filter set ried out in the Gulf of Naples (Mediterranean Sea) 487901. Small amounts of cultures containing sexual stages showed that distinct internal transcribed spacer (ITS) were prepared for SEM as described below. Four F1 generation strains (Table 1) from each of two cross- types are present within P. delicatissima (Orsini et al. ing experiments (P1 Â P2 and P3 Â P4) and three from an- 2004). The ITS types are indistinguishable in the light other crossing experiment (P2 Â P4) were established by the microscope, and two of them share the same TEM isolation of a single initial cell within a day of the completion of ultrastructure previously reported for P. delicatissima auxospore expansion. These strains were crossed among each (Hasle and Syvertsen 1997, Skov et al. 1999); a third other and with the parental strains to test their reproductive ITS type can be differentiated by a slightly different success. Experiments were carried out using the same protocol as described above. arrangement of the poroids on the valve surface. The EM preparations. Subsamples of all parental strains used different genotypes might represent cryptic ‘‘biologi- for mating experiments, of selected strains of the F1 gener- cal’’ species; that is, although they may share the same ation, and of strains obtained from additional crosses were or very similar ultrastructural characters, they might prepared for TEM as described by Orsini et al. (2004) and be reproductively isolated (Mann 1999). Mating ex- observed with an EM 400 microscope (Philips, Eindhoven, periments should be carried out to test this hypothesis. We report here on an investigation of several strains belonging to the most abundant ITS type recorded in TABLE 1. Strains of Pseudo-nitzschia delicatissima used. our area (Orsini et al. 2004). The aim was to describe the sexual cycle in light microscopy (LM) and scanning
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