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Pfiesteria Piscicida (Dinophyceae)1 J. Phycol. 45, 1315–1322 (2009) Ó 2009 Phycological Society of America DOI: 10.1111/j.1529-8817.2009.00754.x GENETIC VARIATION AMONG STRAINS OF PSEUDOPFIESTERIA SHUMWAYAE AND PFIESTERIA PISCICIDA (DINOPHYCEAE)1 Hamish J. Small 2, Jeffrey D. Shields, Leonard W. Haas, Wolfgang K. Vogelbein, Jessica Moss, and Kimberly S. Reece Department of Environmental & Aquatic Animal Health, Virginia Institute of Marine Science, The College of William and Mary, P.O. Box 1346, Gloucester Point, Virginia, 23062-1346, USA The putatively toxic dinoflagellates Pseudopfiesteria ent gel electrophoresis; Exo I, Exonuclease I; shumwayae (Glasgow et J. M. Burkh.) Litaker, Steid., ITS, internal transcribed spacer; NCBI, National P. L. Mason, Shields et P. A. Tester and Pfiesteria Center for Biotechnology Information; PLDs, piscicida Steid. et J. M. Burkh. have been implicated Pfiesteria–like dinoflagellates; SAP, shrimp alka- in massive fish kills and of having negative impacts line phosphatase; SNP, single nucleotide poly- on human health along the mid-Atlantic seaboard of morphism; VIMS, Virginia Institute of Marine the USA. Considerable debate still remains as to the Science mechanisms responsible for fish mortality (toxicity vs. micropredation) caused by these dinoflagellates. Genetic differences among these cultures have not P. shumwayae and P. piscicida are estuarine dinofla- been adequately investigated and may account for gellates that have been associated with fish-kill events or correlate with phenotypic variability among and presumptive impacts on human health within strains within each species. Genetic variation among several estuarine systems along the eastern sea- strains of Ps. shumwayae and P. piscicida was exam- board of the United States (Burkholder et al. 1992, ined by PCR–RFLP analysis using cultures obtained 1995, Glasgow et al. 1995, Steidinger et al. 1996, from the Provasoli-Guillard National Center for Cul- Burkholder and Glasgow 1997, Grattan et al. ture of Marine Phytoplankton (CCMP), as well as 1998). Their distribution appears to be worldwide those from our own and other colleagues’ collection (Jakobsen et al. 2002, Rhodes et al. 2002, 2006, efforts. Examination of restriction digest banding Rublee et al. 2005, Park et al. 2007a,b). The field of profiles for 22 strains of Ps. shumwayae revealed the research on Ps. shumwayae and P. piscicida has been presence of 10 polymorphic restriction endonucle- beset by considerable debate on two fundamental ase sites within the first and second internal tran- properties of these organisms, the mechanism(s) scribed spacers (ITS1 and ITS2) and the 5.8S gene responsible for fish mortality (dinoflagellate toxicity of the rDNA complex, and the cytochrome oxidase vs. micropredation) (Burkholder et al. 1992, Burk- subunit I (COI) gene. Three compound genotypes holder and Glasgow 1997, Burkholder 1999, Vogel- were represented within the 22 Ps. shumwayae bein et al. 2002, Lovko et al. 2003) and the capacity strains. Conversely, PCR–RFLP examination of 14 for stage transformations during the life cycle strains of P. piscicida at the same ITS1, 5.8S, and (Burkholder and Glasgow 1997, 2002, Litaker et al. ITS2 regions revealed only one variable restriction 2002a,b, Peglar et al. 2004). Although these organ- endonuclease site, located in the ITS1 region. In isms have been documented and discussed at length addition, a dinoflagellate culture listed as P. piscicida in the literature, strain variability in Ps. shumwayae (CCMP 1928) and analyzed as part of this study was and P. piscicida has rarely been considered. identified as closely related to Luciella masanensis A diverse capacity for toxin expression (Tox-A, P. L. Mason, H. J. Jeong, Litaker, Reece et Steid. Tox-B, and noninducible) has been reported, and Key index words: COI; genetic variation; PCR– toxigenicity in some strains is suggested to be regu- RFLP; Pfiesteria piscicida; Pseudopfiesteria shu- lated by nutritional status of the culture (Burkhold- mwayae; ribosomal genes er et al. 2001a,b). However, the definition for toxicity remains ambiguous, and many strains have Abbreviations: BLAST, basic local alignment not been tested adequately. In addition, variations search tool; bp, base pair; CCMP, Provasoli- in micropredation behavior among species and Guillard National Center for Culture of Marine strains of Ps. shumwayae and P. piscicida have been Phytoplankton; COI, cytochrome oxidase subunit observed (Lovko et al. 2003). It is evident from a I; CYTB, cytochrome b; DGGE, denaturing gradi- review of the literature that several research groups have conducted experiments with different strains 1Received 10 September 2008. Accepted 6 May 2009. of Ps. shumwayae and P. piscicida and have reported 2Author for correspondence: e-mail [email protected]. different modes of pathogenicity; this highlights the 1315 1316 HAMISH J. SMALL ET AL. need for genetic characterization of these strains to from the food source and maximize capture of Ps. shumwayae interpret and compare experimental results more and P. piscicida cells. DNA extraction. Aliquots of 20 mL of each culture accurately. ) (2 · 103 cells Æ mL 1) were filtered onto a 3 lm Nucleopore Strain variation is a common feature in many algal (Costar, Cambridge, MA, USA) filter to concentrate the cells. species (Scholin and Anderson 1996, Bolch et al. As a control for PCR amplifications, 15 mL of Rhodomonas sp. 1999), especially with regard to toxin expression (CCMP 767) was also filtered (as above). Genomic DNA was (Cembella et al. 2002, Wang et al. 2005) and genetic extracted from the filters using a DNeasy Tissue Kit (Qiagen, variation (Bolch et al. 1999, Evans et al. 2004, Gomez Valencia, CA, USA) following the manufacturer’s protocol. and Gonzalez 2004, Martı´nez et al. 2006). Scholin Purified DNA was eluted into 50 lL of the supplied extraction et al. (1994) and Higman et al. (2001) reported that buffer, quantified using a Hoefer DyNA Quant 200 fluorometer (Pharmacia Biotech Inc., Piscataway, NJ, USA) and stored at toxic and nontoxic species of Pseudonitzschia and )20°C. strains of Alexandrium tamarense were distinguishable PCR amplification. Several sets of primers were designed by analysis of rDNA sequences. Nucleotide poly- (Table 1) based on DNA sequences available in our laboratory morphisms in the ITS regions (and 5.8S rDNA database and in GenBank to target the rDNA regions genes) of both Ps. shumwayae and P. piscicida have (ITS1 ⁄ 5.8S ⁄ ITS2), the COI gene, and other regions of Ps. been recorded previously (Litaker et al. 2003, 2007). shumwayae and P. piscicida genomes, such as the cytochrome b (CYTB) gene of P. piscicida (see Results and Discussion). The In contrast, Tengs et al. (2003) observed no differ- amplification reactions contained 10 mM Tris-HCl, pH 8.3, ences in the ITS1 and ITS2 regions, and the 5.8S 50 mM KCl, 1.5 mM MgCl2, 0.1 mM of each dNTP, 2.5 lMof gene, among isolates of P. piscicida, while Marshall each primer, 1 unit of Taq polymerase (Applied Biosystems, ) et al. (2006) reported finding no differences in Foster City, CA, USA), 0.4 mg Æ mL 1 BSA, and 30–50 ng the 5.8S rDNA gene between several strains of genomic DNA in a total volume of 20 lL. The following cycling Ps. shumwayae, and a 1 bp difference between isolates conditions were used for each locus: an initial denaturation at 94°C for 4 min, followed by 40 cycles of 94°C for 30 s, 30 s at of P. piscicida. the annealing temperature (varied with primers used, see In the current study, we describe the analysis of 22 Table 1), 72°C for 90 s, and a final extension step of 72°C for strains of Ps. shumwayae and 14 strains of P. piscicida 5 min. To check for uniform amplification across all samples, by PCR–RFLP analysis of the ITS1, 5.8S gene, 5 lL aliquots of the amplified products were visualized by and ITS2 rDNA regions, and the cytochrome oxi- agarose gel electrophoresis (2% w ⁄ v), stained with ethidium dase subunit I (COI) gene. Our objective was to bromide, and viewed under a UV light source. Amplification develop a simple method to genotype Ps. shumwayae products selected for sequence analysis were excised from the agarose gels using a sterile scalpel blade and purified using a and P. piscicida isolates and examine whether genetic Qiaquick Gel Extraction Kit (Qiagen). differences exist between geographically separate Sequencing of amplification products. Amplification products isolates. from a number of primary PCRs were cloned and sequenced to confirm that the correct target was amplified. Cloning and MATERIALS AND METHODS sequencing were performed according to methods described previously (Small et al. 2007). Briefly, purified PCR products Cultures. Clonal cultures of Ps. shumwayae and P. piscicida were cloned into the plasmid pCRÒ4-TOPOÒ (Invitrogen, were obtained from the CCMP and through our own and other Carlsbad, CA, USA) and transformed into competent Escheri- colleagues’ sampling efforts. The cells were cultured in sterile chia coli using a TOPO TA CloningÒ Kit (Invitrogen) following Gulf Stream water diluted to 15 psu, at 23°C under a 14:10 the manufacturer’s protocols. Transformed bacterial colonies light:dark (L:D) cycle. All species were fed small amounts of were screened for inserts using a PCR-based screening reaction Rhodomonas sp. (CCMP 767) every 2–3 d. Prior to filtering the using M13 primers (M13F 5¢-GTAAAACGACGGCCAG-3¢ and cells for DNA extraction, the dinoflagellates were allowed to M13R 5¢-CAGGAAACAGCTATGAC-3¢). Aliquots of 3 lLof graze down the Rhodomonas to minimize the DNA obtained all PCR products were analyzed on an agarose
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