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Ecophysiological Characterization of Two Life Forms, Resting Spores and Resting Cells, of a Marine Planktonic Diatom, Chaetocero

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Ecophysiological Characterization of Two Life Forms, Resting Spores and Resting Cells, of a Marine Planktonic Diatom, Chaetocero l MARINE ECOLOGY PROGRESS SERIES Vol. 102: 245-255, 1993 Published December 30 Mar. Ecol. Prog. Ser. Ecophysiological characterization of two life forms, resting spores and resting cells, of a marine planktonic diatom, Chaetoceros pseudocurvisetus, formed under nutrient depletion A. Kuwata l, T. ~ama2, M. Takahashi 'Botany Department, University of Tokyo, Hongo, Tokyo 113, Japan 21nstitute for Hydrospheric-Atmospheric Sciences, Nagoya University, Chikusa-ku, Nagoya 464-01, Japan ABSTRACT: Ecophysiological characteristics of 2 life forms, resting spores and resting cells, produced from vegetative cells of the marine d~atomChaetoceros pseudocurvisetus (Mangin) under nitrogen depletion were ~nvestigated.Carbon and sillcon were concentrated In resting spores to a greater extent than nltrogen and chlorophyll a (chl a) although the levels of nitrogen and chl a were similar to those in vegetative cells. Resting cells were similar in appearance to vegetative cells but with weakly pig- mented, shrunken and fragmented chloroplasts, and contained slightly more slllcon, reduced nitrogen and chl a and similar amounts of carbon in comparison with the vegetative cells. Respiratory and photosynthetic activity was depressed In both resting spores and resting cells. Net photosynthesis was slightly positive in resting spores and slightly negative In resting cells. Both resting spores and rest~ng cells accumulated neutral lipids mainly composed of myristic (C,, "), palmitic (Cle0)and palmtoleic (C,,; ,) acids as a stored energy source with increased unsaturation of fatty acids. Resting spores also stored large amounts of glucose in reserved polysacchandes These charactenstics indicate that each life form represents a different degree of the adaptive restlng stage for survival under nutnent depletion KEY WORDS- Chemical colnposition . Diatom . Metabolic actlvity . Nutrient deficiency . Restlng cell . Rest~ngspore . Survival stage INTRODUCTION many planktonic algae under fluctuating nutrient con- ditions in the marine environment, some mechanisms Under fluctuating natural environments with various may exist. In fact, several species of marine planktonic temporal and spatial scales, each planktonic algal diatoms have been found to form resting spores associ- population is expected to be exposed to both favorable ated with nutrient depletion (Drebes 1966, Davis et al. and unfavorable conditions for growth and reproduc- 1980, Garrison 1981, Ishizaka et al. 1987, Kuwata & tion. Since planktonic algae are not mobile enough to Takahashl 1990). Furthermore, Kuwata & Takahashi select favorable conditions and to avoid unfavorable (1990) have revealed that, in a planktonic diatom conditions by themselves, their lives will be strongly Chaetocel-OS pseudocurvisetus Mangin population, affected by environmental fluctuations. For each resting spore formation induced by nitrogen depletion planktonic algal species to maintain population levels requires a large amount of silicon, and that a part of during such environmental fluctuations, it is essential the algal population which fails to form resting spores to survive under unfavorable conditions as well as to remains vegetative looking with weakly pigmented, grow actively under favorable conditions. shrunken and fragmented chloroplasts, as observed by Nutrient depletion is a harsh condition to which Holmes (1966) under insufficient supply of silicic acid. planktonic algae are occasionally or even frequently Chaetoceros pseudocurvisetus was originally de- exposed in the sea. For the successful establishment of scribed as a tropical or subtropical species (Cupp O Inter-Research 1993 Mar. Ecol. Prog. Ser. 102: 245-255, 1993 1943). This species has recently been observed fre- resting spores and 10 pM nitrate and 20 yM sillcic acid quently in warm waters in the Japanese coastal region for vegetative-looking cells. Samples of vegetative and its bloom has been reported to be common in some cells were cultured in a modified f/2 medium contain- bays from autumn to spring (Takano 1990). It has also ing nitrate (20 FM) and silicic acid (160 PM). been found in locally upwelling water frequently Culture media in polycarbonate bottles were auto- occurring in the Izu Islands, Japan, where the nutrient claved at 120°C under 2 atm, and cooled at least for environment changed greatly from eutrophy to oligo- 24 h at room temperature after autoclaving and before trophy within several days (Takahashi et al. 1986, inoculating cells at the logarithmic growth phase at an Kuwata & Takahashi 1990). initial concentration of ca 30 cells ml-'. All the cultures Considering the actual concurrence of both resting were preincubated for 1 d. spores and such vegetative-looking cells of this algal Samples for cell counting were all fixed with glu- population in oligotrophic water, each life form might taraldehyde (2.5% v/v) and settled in chambers before exhibit resting stages capable of surviving under nutri- counting with an inverted microscope (Utermohl ent depletion, which play an important role for survival 1958). Cell volume was estimated using the equation of in natural water. To verify this possibility, ecophysio- Miyai et al. (1988) from cell length and width deter- logical characterization of both resting spores and mined with 200 preserved cells for each sample, vegetative-looking cells is required. However, there assuming an elliptical cylindrical shape for vegetative have been only a few studies evaluating some charac- and vegetative-looking cells and an ellipsoidal shape teristics of resting spores and vegetative cells of diatom for resting spores. Each sample for nutrient analysis species (French & Hargraves 1980, Doucette & Fryxell was filtered through a cellulose acetate filter (Advan- 1983). tec, DISMIC-25cs) and nitrate and silicic acid deter- In this study, resting spores and vegetative-looking mined colorimetrically according to Strickland & Par- resting cells of Chaetoceros pseudocurvisetus are com- sons (1972). Samples for chemical analyses of resting pared to vegetative cells with regard to survival under spores were collected from culture on Day 8 and those nutrient deficiency. Since reduction of metabolic activ- of vegetative-looking cells on Day 9 after inoculation ity and storage of energy were considered to be essen- into a fresh medium. Vegetative cells were harvested tial for the survival of many organisms (Sussman & during the logarithmic growth phase on Day 4. Douhit 1973), particular attention was paid to changes Metabolic rate measurements. Rates of photosyn- in metabolic activity and chemical composition during thesis and dark respiration were determined by oxy- the transition from vegetative cells to resting spores gen changes using the dark and light bottle method or vegetative-looking cells formed under nutrient with the Winkler titration. Vegetative-looking cells depletion. and resting spores were prepared in the modified f/2 media as mentioned above. Vegetative cells were pre- pared in the medium containing initial concentrations MATERIALS AND METHODS of 50 pM nitrate and 150 pM silicic acid. To avoid over- estimation of respiratory activity due to contamination Preparation of 3 life forms by laboratory culture. by bacteria, preculture for resting cells and resting Isolation of the unialgal strain of Chaetoceros pseudo- spores was rendered axenic by treatments with peni- curvisetus and maintenance of culture were described cillin and streptomycin (Hoshaw & Rosowski 1973). previously (Kuwata & Takahashi 1990). Vegetative cells were harvested during the logarithmic Algal samples were prepared in batch culture using growth phase. Resting cells were taken 2 d after enter- 8 1 polycarbonate bottles at 24 f lS°C under a 14 h ing the stationary phase. Resting spores were obtained light: l0 h dark lighting cycle (ca 600 pm01 m-' S-' 4 to 6 d after their formation. Five bottles each were provided by daylight-type fluorescent tubes). Accord- prepared for light, dark and control treatments. Two ing to the previous study (Kuwata & Takahashi 1990),a 100 m1 bottles were treated as light bottles, and the Chaetoceros pseudocurvisetus population produces changes in chl a and cell concentrations were deter- almost solely resting spores under depletion of nitro- mined during the incubation. All the light and dark genous nutrients with enough silicic acid (required bottles were incubated for 3 h for vegetative cells, and Si/N molar ratio >9.3) or produces only vegetative- for 14 h for resting cells and resting spores at 25OC. looking resting cells under concomitant deficiency of Light bottles were incubated under saturated light silicic acid and nitrogenous nutrients (required SUN intensity p200 pm01 m-2 S-') for photosynthesis pro- molar ratio <3.1).To obtain the 2 different types of life vided by daylight-type fluorescent tubes. form separately under nitrogen deficiency, the cells Chemical analyses. Cellular organic carbon and were grown in modified f/2 medium (Guillard & Ryther nitrogen contents were determined with a CN ana- 1962) with 10 yM nitrate and 140 pM silicic acid for lyzer (Sumlgraph NC80) by filtering algal cell samples Kuwata et al.: Characterization of diatom resting spores and resting cells 247 on a Whatman GF/C glass fiber filter precombusted at column, the wall coated with fused silica (OV-1701, 400 "C. Cellular silicon content was determined using 25 m X 0.25 mm i.d.; GL Science), was used with N2 as the method of Paasche (1980) by filtering algal samples carrier gas. Oven temperature was programmed
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