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Mixotrophy Among Dinoflagellates1 J Eukaryn Microbiol.. 46(4). 1999 pp. 397-401 0 1999 by the Society of Protozoologists Mixotrophy among Dinoflagellates’ DIANE K. STOECKER University of Maryland Center for Environmentul Science, Horn Point Laboratory, P.O. Box 775, Cambridge, Marylund 21613, USA ABSTRACT. Mixotrophy, used herein for the combination of phototrophy and phagotrophy, is widespread among dinoflagellates. It occurs among most, perhaps all, of the extant orders, including the Prorocentrales, Dinophysiales, Gymnodiniales, Noctilucales, Gon- yaulacales, Peridiniales, Blastodiniales, Phytodiniales, and Dinamoebales. Many cases of mixotrophy among dinoflagellates are probably undocumented. Primarily photosynthetic dinoflagellates with their “own” plastids can often supplement their nutrition by preying on other cells. Some primarily phagotrophic species are photosynthetic due to the presence of kleptochloroplasts or algal endosymbionts. Some parasitic dinoflagellates have plastids and are probably mixotrophic. For most mixotrophic dinoflagellates, the relative importance of photosynthesis, uptake of dissolved inorganic nutrients, and feeding are unknown. However, it is apparent that mixotrophy has different functions in different physiological types of dinoflagellates. Data on the simultaneous regulation of photosynthesis, assimilation of dissolved inorganic and organic nutrients, and phagotophy by environmental parameters (irradiance, availablity of dissolved nutrients, availability of prey) and by life history events are needed in order to understand the diverse roles of mixotrophy in dinoflagellates. Key Words. Endosymbioses, harmful algal blooms, kleptoplastidy, microbial food web. INOFLAGELLATES have traditionally been categorized Smalley, G. W., unpubl. data) or are specialized predators on D as autotrophic or heterotrophic, based on the presence or particular types of live prey (Bockstahler and Coats 1993a, b; absence of chlorophyll and plastids. It has long been recognized Jacobson and Anderson 1996; Skovgaard 1996a; Smalley, that some photosynthetic dinoflagellates have food vacuoles and Coats and Adam 1999). Conversely, reports of ingestion of bac- feed on other protists (Biecheler 1936, 1952); however, only terial-size prey by dinoflagellates, including photosynthetic spe- recently has the prevalence of feeding among common photo- cies, are questionable because dinoflagellates prey on relatively synthetic dinoflagellates been documented (Bockstahler and large-size particles and absorption of prey on surfaces or uptake Coats 1993b; Jacobson and Anderson 1996; Li et al. 1996; of dissolved label may have confounded the results (Hansen Stoecker et al. 1997). Likewise, it has long been known that 1998; Hansen and Calado 1999). However, many new cases of some dinoflagellates have plastids with pigment and membrane mixotrophy among dinoflagellates remain to be discovered. characteristics not typical of dinoflagellates, but recent inves- Among the Prorocentrales, food vacuoles or the ingestion of tigations have shown that some of these atypical species harbor prey have been observed in one common bloom-forming pho- kleptochloroplasts or algal endosymbionts obtained from non- tosynthetic species, Prorocentrum minimum (Stoecker et al. dinoflagellate prey (Fields and Rhodes 1991; Larsen 1988; Stei- 1997) and in several tropical, benthic Prorocentrum spp. (Table dinger et al. 1996; Steidinger and Tangen 1997; Sweeney 1976). 1). In natural assemblages, ingested cryptophyte material has In some cases, it has been demonstrated that dinoflagellates been observed in up to 50% of the P. minimum cells. In this with kleptochloroplasts are photosynthetically functional (Skov- primarily phototrophic species, feeding may be a response to gaard 1998) or that the dinoflagellates can grow for several days inorganic nutrient limitation during summer stratification of the in the light but not in the dark in the absence of prey, indicating water column (Stoecker et al. 1997). that the plastids/endosymbionts are functional and benefit the Among the Dinophysiales, food vacuoles have been observed host (Fields and Rhodes 1991; Skovgaard 1998; Sweeney in two photosynthetic species, Dinophysis acuminata and D. 1971). However, most cases of feeding by photosynthetic di- nowegica (Jacobson and Andersen 1994). It has been argued noflagellates and of plastid-retention and endosymbiosis in di- that the Dinophysiales are a basically heterotrophic lineage in noflagellates have not been experimentally investigated, and the which some taxa have secondarily acquired photosynthetic or- relative contributions of phototrophy (photosynthesis and up- ganelles or photosynthetic endosymbionts (Schnepf and El- take of inorganic nutrients) and phagotrophy to survival and brachter 1988). Thus, feeding is expected to be common among growth are largely unknown. Mixotrophy (used herein in the the photosynthetic members of this order. restricted sense for the combination of phototropy and phago- Among the Gymnodiniales, there is evidence for mixotrophy trophy) is a common, but physiologically and ecologically di- in many genera (Table I). Amphidinium latum, Amphidinium verse phenomenon among many taxa of marine and freshwater poecilochroum, Gymnodinium acidotum, Gymnodinium ‘graci- protists (Jones 1997; Jones 1994; Raven 1997; Reimann et al. lentum, ’ and possibly Gymnodinium aeruginosum lack their 1995; Sanders 1991; Stoecker 1998). “own” plastids and are phagotrophic, but retain kleptochloro- Mixotrophs are reported among all the major extant orders plasts or reduced algal endosymbionts, which are usually de- of dinoflagellates, although evidence for mixotrophy is stronger rived from their cryptophyte prey (Fields and Rhodes 1991; in some taxa than in others (Table 1). Mixotrophy is often dif- Horiguchi and Pienaar 1992; Larsen 1988; Schnepf, Winter and ficult to detect in dinoflagellates for several reasons. Chloro- Mollenhauer 1989; Skovgaard 1998). Photosynthetic rates plasts may mask food vacuoles and it can be difficult to distin- equivalent to 187% of body C fixed per d have been measured guish food vacuoles from other types of inclusions (reviewed in Gymno. ‘gracilentum’ fed the cryptophyte Rhodornonas. In in Li et al. 1996; Gaines and Elbrachter 1987; Hansen 1998; the absence of prey, both growth and photosynthetic rates de- Hansen and Calado 1999). Experimentally, it is often difficult crease to near zero within two days in this dinoflagellate (Skov- to induce feeding in mixotrophic dinoflagellates because some gaard 1998). In this case of mixotrophy, the dinoflagellate is species only feed under certain conditions or have low feeding dependent on feeding for growth and for replenishment of func- rates (Li et al. 1996; Stoecker et al. 1997; Li, A., unpubl. data; tional plastids. Photosynthesis by kleptochloroplasts is thought to increase growth and survival during starvation in Gymno. ‘gracilentum’. Corresponding Author: D. Stoecker-Telephone number: 4 10-22 1- 8407; FAX number: 410-221 -8490; e-mail: [email protected] Among the Gymnodiniales, some photosynthetic species with I Symposium presentation for a joint meeting of the Society of Pro- their own plastids are capable of phagotrophy. Amphidinium tozoologists, American Phycological Society, and the International So- cryophilum ingests other dinoflagellates (Wilcox and Wede- ciety of Evolutionary Protistology, August 7, 1998, Flagstaff, AR. mayer 199 1). Gymnodinium sanguineum, Gyrodinium instria- 397 398 J. EUKARYOT. MICROBIOL., VOL. 46, NO. 4, JULY-AUGUST 1999 Table 1. Confirmed or suspected cases of mixotrophy in dinoflagellates.” Taxa Habitat Evidence Reference PROROCENTRALES Prorocentrum micam Mar’ Photosynthetic, observation of microtubular basket Schnepf and Winter 1990 P. minimum Mar Photosynthetic, ingestion of cryptophytes and fluo- Li et al. 1996; Stoecker et al. 1997 rescently labelled prey P. belizeunum Mar Photosynthetic, observation of food vacuoles Faust 1998 P. hoffmannianum Mar Photosynthetic, observation of food vacuoles Faust 1998 DINOPHY SIALES Dinophysis acuminata Mar Photosynthetic, observation of food vacuoles Jacobson and Andersen 1994 D. norvegica Mar Photosynthetic, observation of food vacuoles Jacobson and Andersen 1994 GYMNODINI ALES Amphidinium cryophilum FW‘ Photosynthetic, ingestion of other dinoflagellates Wilcox and Wedemayer 1991 Amphi. latum Mar Phagotrophic, observation of kleptochloroplasts Horiguchi and Pienaar 1992 Amphi. poecilochroum Mar Phagotrophic, observation of kleptochloroplasts Larsen 1988 Gymnodinium acidotum FW Phagotrophic, observation of algal endosymbionts/ Fields and Rhodes 1991 kleptochloroplasts Gymno. aeruginosum FW Phagotrophic, observation of algal endosymbiontsl Schnepf, Winter, and Mollenhauer 1989 kleptochloroplasts Gymno. ‘gracilentum’ Mar Phagotrophic, photosynthetic due to kleptochloro- Skovgaard 1998 plasts Gymno. sanguineum Mar Photosynthetic, observation of food vacuoles, inges- Bockstahler and Coats 19931, b tion of small choreotrich ciliates Gyrodinium galatheanum Mar Photosynthetic, observation of food vacuoles and Li et al. 1996 (as Gymno. Estuariale) ingestion of cryptophytes and other small protists Gyro. instriaturn Mar Photosynthetic, ingestion of tintinnids Uchida, Kamiyama, and Matsuyama 1997 Gyro. pavillardi Mar Photosynthetic, ingestion of ciliates & dinoflagel- Biecheler 1936; Biecheler 1952 lates Gyro. uncatenum Mar Photosynthetic, observation of food vacuoles with Bockstahler and Coats 1993b choreotrich ciliates Torodinium teredo Mar Observation
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