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Auxospore Formation by the Silica-Sinking, Oceanic Diatom Fragilariopsis Kerguelensis (Bacillariophyceae)1

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Auxospore Formation by the Silica-Sinking, Oceanic Diatom Fragilariopsis Kerguelensis (Bacillariophyceae)1 J. Phycol. 42, 1002–1006 (2006) r 2006 by the Phycological Society of America DOI: 10.1111/j.1529-8817.2006.00260.x NOTE AUXOSPORE FORMATION BY THE SILICA-SINKING, OCEANIC DIATOM FRAGILARIOPSIS KERGUELENSIS (BACILLARIOPHYCEAE)1 Philipp Assmy2, Joachim Henjes, Victor Smetacek Alfred Wegener Institute for Polar and Marine Research, Am Handelshafen 12, 27570 Bremerhaven, Germany and Marina Montresor Stazione Zoologica ‘‘A. Dohrn’’, Villa Comunale, 80121 Napoli, Italy Size restoration by the auxospore that develops central role played by the sexual phase in the diatom from the zygote is a crucial stage in diatom life life history dictated by its peculiar cell morphology. cycles. However, information on sexual events in Diatom cells are enclosed in two siliceous thecae and pelagic diatom species is very limited. We report for during mitotic division each daughter cell retains one the first time auxospore formation by the pennate maternal theca and synthesizes a new one internally. It diatom Fragilariopsis kerguelensis (O’Hara) Hustedt follows that the two daughter cells differ slightly in size, during an iron-induced bloom in the Southern which causes a progressive reduction of the average Ocean (EIFEX, European Iron Fertilization EXper- cell size in a growing population (MacDonald 1869, iment). Auxospores of F. kerguelensis resembled Pfitzer 1869). This progressive size reduction can be those described for Pseudo-nitzschia species. The curtailed by the onset of the sexual cycle and the pro- auxospore was characterized by an outer coating, duction of the auxospore. Within the auxospore, which the perizonium; two caps, one at each distal end; is not surrounded by rigid siliceous thecae, a large- and four chloroplasts, one at each end and two in sized initial cell is formed. Thus, in diatoms, the sexual the central part. Different stages of auxospore elon- phase combines two crucial events of the species life gation were recorded, with a length of 24–91 lm, but cycle: the occurrence of meiosis, and thus genetic re- only the largest auxospores contained the initial combination, and the restoration of large-sized cohorts cell, whose apical axis ranged between 76 and of cells in the population. 90 lm. Gametangial cell walls were often attached We report for the first time on the finding of sexual to the auxospores and ranged from 10 to 31 lmin stages of the pennate diatom Fragilariopsis kerguelensis length. Auxospore abundances were consistently (O’Meara) Hustedt, which is one of the dominant higher in the fertilized patch, where an increase in diatom species of the ice-free Antarctic Circumpolar the F. kerguelensis population was observed, as com- Current (ACC) (Hart 1934, Smetacek et al. 2004). pared with surrounding waters. It forms curved, ribbon-like chains that can be m Key index words: auxospore; diatoms; Fragilario- over 300 m long and is easily differentiated from con- psis kerguelensis; life history; sexual reproduction; generic species occurring in the Southern Ocean by Southern Ocean virtue of its heavily silicified frustules with a low density of well-marked striae (Hasle 1965, Hasle and Syvertsen 1997). The thick frustules are remarkably strong and have likely evolved as mechanical protection against Diatoms are major contributors to marine primary crustacean zooplankton. They hence ensure long-term production and play a key role in the ocean carbon and persistence in the surface layer (Hamm et al. 2003). silica cycles (Smetacek 1999). Although the intricate life F. kerguelensis is a major contributor to the diatom ooze histories of several diatoms have been described forming the Antarctic opal belt (Zielinski and Gersonde (Drebes 1977, Edlund and Stoermer 1997, Chepur- 1997), the largest depot of biogenic silica in the world nov et al. 2004), field observations of sexual stages in ocean (Tre´guer et al. 1995). Thus, its ecological prop- marine planktonic species are extremely scant (Mann erties make F. kerguelensis by far the most important 1988, Jewson 1992a, b, Waite and Harrison 1992, diatom species in the global silicon cycle and an indica- Crawford 1995). This is surprising, considering the tor species of a silica-sinking regime in an otherwise iron-limited ecosystem (Smetacek et al. 2004). 1Received 14 December 2005. Accepted 28 June 2006 Seawater samples were collected during the in situ 2Author for correspondence: e-mail [email protected]. iron fertilization experiment European Iron Fertiliza- 1002 AUXOSPORE FORMATION IN FRAGILARIOPSIS KERGUELENSIS 1003 tion EXperiment (EIFEX) conducted in the Atlantic being immature, having been fixed before expansion Sector of the Southern Ocean (021E, 491S) in late aus- was complete. Initial thecae were present only in tral summer to early austral fall (11 February–19 auxospores that had reached 76–90 mm (aver- March 2004) during cruise ANT XXI-3 of R.V. age 5 84 mm; n 5 18) and we consider this as the size Polarstern (Smetacek 2005). The ‘‘in-patch stations’’ range of mature auxospores. The width of the initial were placed at the sites of the highest photosynthetic thecae varied between 7 and 13 mm. The auxospores efficiency (Fv/Fm) and/or the lowest pCO2 values ob- were slightly inflated in their central part (Fig. 1, c served, hence closest to the center of the iron-fertilized and d). This central bulge was not evident in the initial patch. ‘‘Out-patch stations’’ were located in adjacent, thecae (Fig. 1, d–f), indicating that this feature was not iron-limited waters with low Fv/Fm ratios and equilib- inherited during thecae deposition. The auxospores rium pCO2 concentrations. were delimited by a perizonium consisting of trans- Water samples for the estimation of phytoplankton verse siliceous bands (Fig. 1, c and d) and one cap was cell concentration were obtained from Niskin bottles present at each distal end (Fig. 1d). Auxospores in attached to a conductivity temperature depth (CTD) which the thecae of the initial cell were not yet formed rosette from seven depths between 10 and 150 m at contained four chloroplasts: one at each end and two nine ‘‘in-patch’’ and five ‘‘out-patch’’ stations. Water in the central part of the auxospore (Fig. 1c). In stages samples of 200 mL were preserved with hexamine- in which the deposition of the first theca of the buffered formaldehyde solution at a final concentration initial cell became evident, the four chloroplasts were of 2% and stored at 41 C in the dark for subsequent aligned along the wall (Fig. 1d). The initial thecae were counting in the home laboratory. A volume of 50 mL not formed in contact with the inside of the per- was settled in sedimentation chambers (Hydrobios, izonium (Fig. 1, d and e). In most cases, auxospores Kiel, Germany) for 48 h. Cells and sexual stages were were attached to gametangial thecae. It was thus pos- identified and enumerated using inverted light and sible to estimate the size of the gametangia that ranged epifluorescence microscopes (Axiovert 200 and Axi- from 10 to 31 mm in length (n 5 48). We exclusively overt 135, Zeiss, Oberkochen, Germany) according to observed gametangia bearing only one auxospore the method of Utermo¨hl (1958). Auxospores were pho- and, in a few cases, we observed one auxospore con- tographed and measured with a Zeiss AxioCam MRc5 nected to two gametangial thecae that differed in and the Zeiss AxioVision software 4.1. Auxospore abun- length (Fig. 1b). dances (number of auxospores Á m À 2) were obtained Auxospores of F. kerguelensis were recorded both in- from trapezoidal integration of values from the 100 m side and outside the iron-fertilized patch and through- deep surface mixed layer. out the water column, from the surface to 150 m F. kerguelensis was one of the dominant species dur- depth. Interestingly, one auxospore was even found ing the iron-induced bloom and contributed up to 14% at 1000 m depth. Depth-integrated abundances over of the total diatom biomass (P. Assmy, unpublished the upper 100 m of the water column ranged between data). Cells were mainly joined in chains of variable 1.8 and 11.4 Â 106 auxospores Á m À 2 inside the patch length and were 10–90 mm long (Fig. 1a). In the water and 0–3.5 Â 106 auxospores Á m À 2 outside the patch samples collected during the bloom, we repeatedly re- (Fig. 2). Auxospore abundances were consistently high- corded auxospores of a pennate diatom (Fig. 1, b–e). er inside the patch, in accordance with the iron-induced The identification of these sexual stages as F. kergue- increase of the F. kerguelensis population. Auxospores lensis was unequivocal and based on the fact that au- accounted for 0.03%–0.4% of the total population, with xospores were often still attached to the gametangia the highest relative contribution inside the patch. (Fig. 1b) or that the initial cell was visible inside the F. kerguelensis belongs to the family Bacillariaceae auxospore (Fig. 1e) and after release from the auxo- and is genetically closely related to species of the genus spore (Fig. 1f). It has thus been possible to observe the Pseudo-nitzschia (Lundholm et al. 2002). Its auxospore distinctive morphological features of the vegetative, presents morphological similarities to the auxospores gametangial, and initial cells, which were characterized of Pseudo-nitzschia and those of many other pennate by a low density of striae (4–7 in 10 mm) always clearly diatom species (Fryxell et al. 1991, Davidovich and visible both in girdle view and in cells containing Bates 1998, Kaczmarska et al. 2000, Amato et al. chloroplasts (Fig. 1, a, b, e and f; Hasle 1965, Hasle 2005). These similarities include the presence of a and Syvertsen 1997). Except for a single finding of a transversal perizonium with conspicuous bands and much slimmer auxospore, most probably attributable caps at the extremities of the auxospore.
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