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A025p293.Pdf AQUATIC MICROBIAL ECOLOGY Vol. 25: 293–300, 2001 Published September 28 Aquat Microb Ecol Coupling of thraustochytrids and POM, and of bacterio- and phytoplankton in a semi-enclosed coastal area: implication for different substrate preference by the planktonic decomposers Hiroyuki Kimura, Makoto Sato, Chino Sugiyama, Takeshi Naganuma* School of Biosphere Sciences, Hiroshima University, 1-4-4 Kagamiyama, Higashi-Hiroshima 739-8528, Japan ABSTRACT: Abundances of planktonic thraustochytrids and bacterioplankton were investigated in the Seto Inland Sea, Japan, with reference to concentrations of potential growth substrates such as dissolved organic carbon (DOC) and particulate organic carbon (POC) concentration and of phyto- plankton (chlorophyll a concentration). Thraustochytrid and bacterioplankton cells were stained with acriflavine and acridine orange, respectively, and directly counted by epifluorescence microscopy. Thraustochytrids occurred in the water column at a density of 0.9 × 102 to 2.1 × 104 cells l–1, with an overall average (±SD) of 3.1 ± 4.0 × 103 cells l–1. Bacterioplankton were found in the water column at a density of 1.1 × 109 to 6.6 × 1010 cells l–1, with an overall average of 4.8 ± 7.0 × 109 cell l–1. Thraus- tochytrid abundance was significantly correlated primarily to POC concentration (r = 0.547, p < 0.001) and secondarily to chlorophyll a concentration (r = 0.318, p < 0.001). By contrast, bacterioplankton concentration was significantly correlated primarily to chlorophyll a concentration (r = 0.498, p < 0.001) and secondarily to DOC concentration (r = 0.236, p = 0.002) but negatively to POC concentra- tion (r = 0.143, p = 0.068). Phytoplankton-derived POC accounted for a certain fraction (only ambigu- ously estimated at 20 to 60%) of total POC, and about 20% of POC was ascribable to bacterioplank- ton biomass. The remaining POC was assumed to be non-phytoplanktonic, non-bacterioplanktonic sources such as phytodetritus and terrigenous matter. Therefore, it is suggested that bacterioplank- ton abundance may depend primarily on phytoplankton-derived DOC whereas thraustochytrid abundance is more influenced by non-phytoplankton, non-bacterioplankton POC. That is, planktonic degraders, thraustochytrids and bacterioplankton, decompose substrates of different origins and sizes. The potential ecological importance of the thaustochytrids as active degraders of POC and as an alternative food source is discussed. KEY WORDS: Thraustochytrid · Fungoid protist · Bacterioplankton · Abundance · Particulate organic carbon · Dissolved organic carbon · Chlorophyll a Resale or republication not permitted without written consent of the publisher INTRODUCTION al. 1973). Thraustochytrids are now classified in the phylum Heterokonta within the kingdom Stra- Thraustochytrids are obligately marine- and estuar- menopila (Patterson 1999). The phylum Heterokonta ine-dwelling protists (Moss 1986), and were formerly also includes the species of diatoms and brown algae classified as the lower fungi, heterotrophic eukaryotic as well as the oomycetes (Cavalier-Smith et al. 1994). microorganisms. This group is characterized by the Previous studies have determined the abundance of presence of an ectoplasmic net and a cell wall com- thraustochytrids over a wide range of habitats, includ- posed of non-cellulosic, sulfurylated scales (Darley et ing the water column, algae, particulate detritus and invertebrates (Raghukumar et al. 1990, Riemann & Schaumann 1993, Frank et al. 1994, Naganuma et al. *Corresponding author. E-mail: [email protected] 1998, Kimura et al. 1999). A rapid direct detection tech- © Inter-Research 2001 294 Aquat Microb Ecol 25: 293–300, 2001 nique using the fluorogenic dye acriflavine was devel- kumar & Raghukumar 1999) and plant material such as oped and used for the enumeration of thraustochytrids algal tissue (Miller & Jones 1983, Sathe-Pathak et al. (Raghukumar & Schaumann 1993). The acriflavine flu- 1993, Sharma et al. 1994), cellulosic material (Fell & orescence technique relies on the fact that the wall and Master 1973, Findlay et al. 1986) and mangrove leaf nucleus of thraustochytrid cell fluoresce differently in (Ulken 1984, Raghukumar 1988, Raghukumar et al. red and blue-green, respectively, under blue-light 1994, Bremer 1995). These observations suggest that excitation. This dual fluorescence distinguishes thraus- thraustochytrids may play a definite role in the dynam- tochytrids from other protists and detritus. In recent ics of particulate organic matter (POM) in the marine studies, 18S rDNA analysis identified thraustochytrids ecosystem. On the other hand, it is known that dis- in the pico- and nanoplanktonic assemblages from the solved organic matter (DOM), such as exudate DOM equatorial Pacific Ocean and the Antarctic polar front from phytoplankton (Larsson & Hagström 1979) and (López-García et al. 2001, Moon-van der Staay et al. terrigenous DOM in river water (Zweifel et al. 1995, 2001). Note that the enumeration based on acriflavin- Kuparinen et al. 1996, Rolff & Elmgren 2000), is used as staining may include protozoan cysts (leading to over- a growth substrate for bacterioplankton (Zweifel et al. estimation) and exclude thraustochytrid zoospores 1993, Moran & Hodson 1994, Hullar et al. 1996). (leading to underestimation). Contribution of this over- However, no work has been published on the correla- and underestimation should be evaluated in future tion between the abundances of planktonic thrausto- studies by using a more specific technique such as chytrids and bacterioplankton and the concentrations immunofluorescence microscopy. of dissolved organic carbon (DOC), particulate organic The fungoid protists, thraustochytrids, are sized carbon (POC) and chlorophyll a (chl a). largely between 3.5 and 20 µm in diameter (Raghuku- We report the distribution of planktonic thraus- mar & Schaumann 1993, Naganuma et al. 1998), and tochytrids and bacterioplankton abundances in the are larger than bacterioplankton (<1 µm, Naganuma & Seto Inland Sea and their correlation with DOC, POC Miura 1997). Thus, thraustochytrids are thought to and chl a concentrations. serve as important food sources for picoplankton feed- ers and contribute to the increase in the efficiency of pelagic secondary production (Naganuma et al. 1998, MATERIALS AND METHODS Kimura et al. 1999). Thaustochytrids uniquely produce polyunsaturated fatty acids such as docosapentaenoic Sample collection and site description. In total, 165 acid and docosahexaenoic acid (Nakahara et al. 1996), water samples were collected for determining the which may be important nutritionally for the growth of abundances of thraustochytrids and bacterioplankton fish larvae (Raghukumar 1986, Raghukumar & Bala- and the concentrations of DOC, POC and chl a. Sam- subramian 1991). ples were collected with Van Dorn samplers from 42 Another ecological role of thraustochytrids is decom- sites at 3 depths (1, 5 and 15 m) during cruises by RV position of refractory organic substrates in marine ‘Toyoshio-maru’ in July and September 2000. The ecosystems (Perkins 1973). Thraustochytrids have samples were collected in the Seto Inland Sea and the been reported to occur in association with decaying Hyuga Nada area, Japan (Table 1, Fig. 1). The Van fecal pellets of zooplankton such as salps (Raghu- Dorn samplers were pre-washed and pre-rinsed with distilled water, and re-washed with Table 1. Sites and months of sample collection, corresponding area names, and seawater of the same site and depth range of surface water temperature observed during each cruise (July and Sep- immediately before sample collection. tember 2000). –: samples were not collected; +: samples were collected Vertical profiles of water tempera- ture, salinity and dissolved oxygen Site no. Area name Jul 2000 Sep 2000 were monitored at each sampling 15.1–29.0°C 23.1–27.6°C site with a Sea Bird conductivity, temperature, depth profiler (CTD). 1 to 3 Hyuga Nada Kuroshio-affecteda –+ Water temperature ranged from 4 Bungo Channel Outer Seto Inland Sea – + 5 to 14 Iyo Nada Seto Inland Sea + + 15.1°C (Site 6, 15 m depth) to 29.0°C 15 to 17 Hiroshima Bay Seto Inland Sea + + (Site 20, 1 m depth) in July, and 18 to 22 Hiuchi Nada Seto Inland Sea + – from 23.1°C (Site 11, 15 m depth) 23 Bisan Seto Seto Inland Sea + – to 27.6°C (Site 1, 1 m depth) in 24 to 29 Harima Nada Seto Inland Sea + – 30 to 37 Osaka Bay Seto Inland Sea + – September. Salinity ranged from 38 to 42 Kii Channel Seto Inland Sea + – 27.2 psu (Site 34, 1 m depth) to aKuroshio Current, NW Pacific 33.9 psu (Site 33, 15 m depth) in July, and from 30.7 psu (Site 17, 1 m Kimura et al.: Distribution of planktonic thraustochytrids and bacterioplankton abundances 295 Fig. 1. Site locations of sample collection in and near the Seto Inland Sea, Japan depth) to 34.2 psu (Site 1, 15 m depth) in September. The limitation of the current staining technique is Dissolved oxygen concentration was within the range that zoospores of most thraustochytrid species lack cell –1 from 2.64 mg O2 l (Site 37, 15 m depth) to 5.23 mg walls (Moss 1986). Also, very small cells (<5 µm) were –1 O2 l (Site 17, 1 m depth) in July, and from 2.81 mg not easily distinguishable because the cell wall-associ- –1 –1 O2 l (Site 17, 15 m depth) to 4.90 mg O2 l (Site 17, ated red fluorescence was weaker than the nucleus- 1 m depth) in September. associated green fluorescence. Thus, very small cells Thraustochytrid and bacterial cell staining and were not counted, and the counts reported in this study counting. Planktonic thraustochytrid and bacterial probably are underestimations. cells were collected on pre-blackened polycarbonate Determination of DOC, POC and chl a concentra- filters (Isopore, Millipore; pore size, 0.2 µm; diameter, tions. Immediately after sampling, 200 ml of water 25 mm) immediately after water collection. Each 10 to samples was filtered through pre-combusted glass 20 ml of sample water was filtered for thraustochytrid fiber filters (450°C, 3 h; 25 mm, Whatman GF/F), and cell counts, and each 0.5 to 2 ml was filtered for bacte- both filtrate and filters were kept frozen at –20°C until rial cell counts.
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