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Inducible Mixotrophy in the Dinoflagellate Prorocentrum Minimum

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Inducible Mixotrophy in the Dinoflagellate Prorocentrum Minimum The Journal of Published by the International Society of Eukaryotic Microbiology Protistologists Journal of Eukaryotic Microbiology ISSN 1066-5234 ORIGINAL ARTICLE Inducible Mixotrophy in the Dinoflagellate Prorocentrum minimum Matthew D. Johnson Woods Hole Oceanographic Institution, 266 Woods Hole Road, Woods Hole, Massachusetts, 02543 Keywords ABSTRACT Alveolate; cryptophyte; grazing; nutrient starvation; phagotrophic phototroph; stress; Prorocentrum minimum is a neritic dinoflagellate that forms seasonal blooms Teleaulax amphioxeia. and red tides in estuarine ecosystems. While known to be mixotrophic, previ- ous attempts to document feeding on algal prey have yielded low grazing Correspondence rates. In this study, growth and ingestion rates of P. minimum were measured M.D. Johnson, Biology Department, Woods as a function of nitrogen (-N) and phosphorous (-P) starvation. A P. minimum Hole Oceanographic Institution, 266 Woods isolate from Chesapeake Bay was found to ingest cryptophyte prey when in Hole Road, Woods Hole, MA 02543, USA stationary phase and when starved of N or P. Prorocentrum minimum ingested Telephone number: +1(508) 289-2584; two strains of Teleaulax amphioxeia at higher rates than six other cryptophyte FAX number: +1(508) 289-457-2076; species. In all cases -P treatments resulted in the highest grazing. Ingestion e-mail: [email protected] rates of -P cells on T. amphioxeia saturated at ~5 prey per predator per day, while ingestion by -N cells saturated at 1 prey per predator per day. In the Received: 22 August 2014; revised 12 presence of prey, -P treated cells reached a maximum mixotrophic growth rate November 2014; accepted November 12, À1 À1 (lmax) of 0.5 d , while -N cells had a lmax of 0.18 d . Calculations of 2014. ingested C, N, and P due to feeding on T. amphioxeia revealed that phagotro- phy can be an important source of all three elements. While P. minimum is a doi:10.1111/jeu.12198 proficient phototroph, inducible phagotrophy is an important nutritional source for this dinoflagellate. MIXOTROPHY is a widely practiced nutritional mode for 1998; Stoecker et al. 2009). Phagotrophy is an ancestral marine protists that combines phagotrophic heterotrophy trait that persists in all eukaryotic supergroups, and con- and photoautotrophy (Jones 1994; Sanders 1991; Stoecker stitutive mixotrophy has been documented within the Stra- 1998). The important ecological role of mixotrophy in pro- menopiles (e.g. chrysophytes), Alveolates (dinoflagellates), viding access to limiting nutrients has long been recog- Haptophytes, Archaeplastids (green algae), and Hacrobians nized (Bird and Kalff 1986; Caron et al. 1990; Keller et al. (cryptophytes). The retention of this trait among plastid- 1994; Nygaard and Tobiesen 1993). In oligotrophic ocean containing protists in marine foodwebs is particularly con- regions, where micro and/or macronutrients are chronically spicuous within the dinoflagellates (Jeong et al. 2010). limiting, bacterivory by mixotrophic flagellates has been Among constitutive mixotrophs, phagotrophy can be shown to be ubiquitous, shaping both the diversity and broadly categorized as being an inducible or persistent productivity of eukaryotic phytoplankton (Hartmann et al. trait, and this phenomenology of feeding reflects its physi- 2012). In coastal ecosystems, mixotrophy can be impor- ological role as either a source for limiting nutrients or as tant for both maximizing growth potential of certain spe- a major nutritional source for maximizing growth. Photo- cies (Li et al. 1999), or as a nutrient source when synthetic and heterotrophic metabolism in mixotrophs is dissolved nutrients are limiting (Smalley et al. 2003). rarely balanced (Flynn and Mitra 2009; Stoecker 1998), Mixotrophy may be divided into two major classes: (1) and the relative importance of each process varies by spe- the phagotrophic phototrophs or constitutive mixotrophs, cies due to factors such as their photosynthetic growth which possess intrinsic plastids and feed to supplement efficiency (Adolf et al. 2006a; Skovgaard et al. 2000) and their nutrition, and (2) photosynthetic protozoa, acquired need for “growth factors” (Skovgaard 2000). phototrophs, or nonconstitutive mixotrophs, which lack The dinoflagellate Prorocentrum minimum has been docu- their own plastids but sequester them from algal prey or mented to form annual blooms in numerous coastal and host endosymbionts (Flynn and Mitra 2009; Stoecker estuarine ecosystems (Glibert et al. 2012; Heil et al. 2005). © 2014 The Author(s) Journal of Eukaryotic Microbiology © 2014 International Society of Protistologists Journal of Eukaryotic Microbiology 2015, 62, 431–443 431 P. minimum Mixotrophy Johnson In Chesapeake Bay P. minimum is transported annually from extracting overnight in 90% acetone at À20 °C, and reading the mouth of the Bay during winter, to the upper bay the sample on a TD-700 (Turner Designs, Sunnyvale, CA) (~240 km) during spring (Tyler and Seliger 1978). Blooms of fluorometer. Photophysiology was evaluated using a fluo- P. minimum in Chesapeake Bay are most frequent between rescence induction and relaxation (FIRe) fluorometer sys- April and May, between temperatures of 12 and 28 °Cand tem (Satlantic, Halifax, NS, Canada). Dark-adapted (15 min) salinities of 4.5–12.8 PSU, and can reach concentrations in samples were put into a cylindrical 1 cm path length cuv- excess of 105 cells/ml (Tango et al. 2005). Nuisance blooms ette and placed in the FIRe fluorometer, where a blue of P. minimum have become more persistent in many tem- (450 nm) LED source was used to analyze samples. This perate estuaries in response to coastal eutrophication (Gli- consisted of a single turnover flash excitation of 80 lsto bert et al. 2012; Heil et al. 2005; Heisler et al. 2008; saturate photosystem II (PSII) and to push fluorescence to a Hodgkiss and Ho 1997; Paerl 1997). The persistence of these maximum, followed by a relaxation sequence that consisted blooms, under high N:P ratios, relative to Redfield propor- of 40 pulses of weak modulated light separated by 60 ls tions, points to flexible nutrient acquisition pathways (Glibert intervals. All curves were fitted using the software FIREP- et al. 2012). In P. minimum these pathways include mixotro- RO (v.1.20, Satlantic, Inc). A summary of how this method- phy (Stoecker et al. 1997), expression of alkaline phospha- ology works and how various physiological parameters are tase during P-starvation (Dyhrman and Palenik 1999), and determined may be found elsewhere (Kolber et al. 1998). ectocellular aminopeptidases that cleave amino acids from Cellular carbon (C), nitrogen (N), and phosphorous (P) dissolved organic matter (Salerno and Stoecker 2009; Stoec- concentrations were determined by filtering 10–30 ml of ker and Gustafson 2003). While previous studies have docu- cells onto a pre-combusted Whatman GF/F filter, for CHN mented mixotrophy in P. minimum in field (Stoecker 1998) and particulate P (PP) analysis. Samples were analyzed and laboratory (Jeong et al. 2005; Salerno 2005) conditions, using a CE-440 Elemental Autoanalyzer (Exeter Analytical details of their grazing kinetics and how feeding relates to Inc., Chelmsford, MA) and a Technicon AutoAnalyzer II nutrient starvation is lacking. The aims of this study were to (SEAL Analytical, Mequon, WI) for CHN and PP analyses, determine: (1) the optimal cryptophyte prey for P. minimum, respectively, at the Analytical Services Department of Uni- (2) the role of inorganic N and P starvation in inducing mixo- versity of Maryland, Center for Environmental Science, trophic feeding, and (3) to determine grazing rates on crypto- Horn Point Laboratory. Cell dimensions for acid Lugol’s phyte prey and its impact on growth of P. minimum. preserved cryptophyte prey were determined using a Ze- iss Axioscope and correcting for the average cell volume shrinkage (Montagnes et al. 1994) MATERIALS AND METHODS Algal cultures Experimental conditions Prorocentrum minimum (CBJR10) was isolated by MDJ Nutrient starvation was induced by transferring log-phase from the mouth of the James River, Chesapeake Bay, dur- P. minimum cells into f/2 (-Si) media without either phos- ing a cruise in October of 2011. Teleaulax amphioxeia phorous (-P treatment) or nitrate (-N treatment), and allow- strains GCEP01 and GCEP02 were isolated from Eel Pond, ing cells to starve under batch culture conditions. Falmouth, MA, in May 2008 by Dr. Mengmeng Tong, Assessment of P. minimum grazing on various crypto- Hanusia phi (CCMP 325), Hemiselis andersenii (CCMP phyte species was determined by adding nutrient replete 439), Guillardia theta (CCMP 2712), Proteomonas sulcata (NR), -P (starved 2 wk), or -N (starved 2 wk) P. minimum (CCMP 704), and Rhodomonas salina (CCMP 757) were to 24-well polystyrene plates in filtered seawater at obtained from the National Center for Marine Algae and 1 9 103 cells/ml, and adding each cryptophyte prey at Microbiota (formally CCMP), and Storeatula major (SM or 1 9 104 cells/ml. After 24 h, 1 ml was removed and fixed g) was isolated from Chesapeake Bay by Dr. Allen Lewitus with 1% gluteraldehyde (Sigma Chemicals, St. Louis, MO) (Table 1). All cultures were maintained in batch at 18 °C, for at least 1 h at 4 °C, filtered onto a black 2.0 lm poly- using f/2 medium (-Si) (Guillard and Ryther 1962) added to carbonate filter under low pressure, mounted on a micro- seawater (35 PSU), 0.2 lm-filtered and autoclaved (FSW), scope slide with fluorescence-grade immersion oil, and collected from Martha’s Vineyard Sound, MA. Irradiance enumerated using a Zeiss AxioScope A1 under blue (Ex: was measured using a QMSW-SS light meter (Spectrum BP 450-490, BS FT 510; Em: LP 515 nm) and green (Ex: Technologies, Inc. Aurora, IL), and maintained at 14:10 h BP 546/12, BS FT 560; Em: BP 575–640 nm) fluorescent light-dark cycle, at 50 lmol photons/m2/s. light. Frequency and number of phycoerythrin-containing food vacuoles in feeding cells, which appear as circular orange bodies, were enumerated. For all prey treatments, Cellular attributes and enumeration at least 300 P. minimum cells were enumerated.
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