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Sequestration, Performance, and Functional Control of Cryptophyte Plastids in the Ciliate Myrionecta Rubra (Ciliophora)1

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Sequestration, Performance, and Functional Control of Cryptophyte Plastids in the Ciliate Myrionecta Rubra (Ciliophora)1 J. Phycol. 42, 1235–1246 (2006) r 2006 by the Phycological Society of America DOI: 10.1111/j.1529-8817.2006.00275.x SEQUESTRATION, PERFORMANCE, AND FUNCTIONAL CONTROL OF CRYPTOPHYTE PLASTIDS IN THE CILIATE MYRIONECTA RUBRA (CILIOPHORA)1 Matthew D. Johnson2 Horn Point Laboratory, Center for Environmental Science, University of Maryland, Cambridge, Maryland 21613, USA Torstein Tengs National Veterinary Institute, Section of Food and Feed Microbiology, Ullevaalsveien 68, 0454 Oslo, Norway David Oldach Institute of Human Virology, School of Medicine, University of Maryland, Baltimore, Maryland, USA and Diane K. Stoecker Horn Point Laboratory, Center for Environmental Science, University of Maryland, Cambridge, Maryland 21613, USA Myrionecta rubra (Lohmann 1908, Jankowski Key index words: ciliate; Geminigera cryophila; 1976) is a photosynthetic ciliate with a global dis- mixotrophy; Myrionecta rubra; nucleomorph; or- tribution in neritic and estuarine habitats and has ganelle sequestration long been recognized to possess organelles of Abbreviations: CMC, chloroplast–mitochondria cryptophycean origin. Here we show, using nucleo- complex; HL, high light; LL, low light; LMWC, morph (Nm) small subunit rRNA gene sequence low-molecular-weight compound; MAA, micros- data, quantitative PCR, and pigment absorption scans, that an M. rubra culture has plastids identi- porine-like amino acids; ML, maximum likelihood; NGC, number of genomes per cell; PE, photosyn- cal to those of its cryptophyte prey, Geminigera thesis versus irradiance; TBR, tree bisection-recon- cf. cryophila (Taylor and Lee 1971, Hill 1991). Using quantitative PCR, we demonstrate that G. cf. struction cryophila plastids undergo division in growing M. rubra and are regulated by the ciliate. M. rubra maintained chl per cell and maximum cellu- Myrionecta rubra (5Mesodinium rubrum) (Lohmann cell lar photosynthetic rates (Pmax) that were 6–8 times 1908, Jankowski 1976) (Mesodiniidae, Litostomatea) that of G. cf. cryophila. While maximum chl-specific is a photosynthetic ciliate with a widespread global chl photosynthetic rates (Pmax) are identical between distribution and is known to cause recurrent red-water the two, M. rubra is less efficient at light harvesting blooms in numerous regions (Taylor et al. 1971, in low light (LL) and has lower overall quantum ef- Lindholm 1985). Photosynthetic measurements dur- ficiency. The photosynthetic saturation parameter ing M. rubra blooms have been among the highest (Ek) was not different between taxa in high light and primary production rates ever measured (Smith and was significantly higher in M. rubra in LL. Lower Barber 1979). Blooms of M. rubra can be massive in C Chl:carbon ratios (h), and hence Pmax rates, in M. scale and highly dynamic in their water column rubra resulted in lower growth rates compared with position (Ryther 1967, Crawford et al. 1997). M. rubra G. cf. cryophila. G. cf. cryophila possessed a greater feeds on cryptophyte algae (Gustafson et al. 2000) and capacity for synthesizing protein from photosynt- possesses plastids, mitochondria (Taylor et al. 1969, hate, while M. rubra used 3.2 times more fixed C for 1971), and nuclei (Hibberd 1977, Oakley and Taylor synthesizing lipids. Although cryptophyte plastids 1978) of cryptophyte origin. in M. rubra may not be permanently genetically in- Unlike most plastid-retaining ciliates, M. rubra is tegrated, they undergo replication and are regu- able to grow phototrophically for long periods without lated by M. rubra, allowing the ciliate to function as feeding on new prey and has the ability to synthesize a phototroph. chl (Gustafson et al. 2000, Johnson and Stoecker 2005). Despite the fact that it ingests cryptophyte algae, M. rubra is generally considered a functional pho- 1Received 21 March 2006. Accepted 10 July 2006. totroph as most of the ingested cryptophyte organelles 2Author for correspondence and present address: Institute of Marine and Coastal Sciences, Rutgers University, 71 Dudley Road, and cytoplasm appear to be retained in membrane- New Brunswick, NJ 08901-8521, USA. E-mail johnson@marine. delineated compartments (Taylor et al. 1969, 1971) rutgers.edu. rather than being digested. Recent estimated C 1235 1236 MATTHEW D. JOHNSON ET AL. budgets for M. rubra suggest that ingested prey C light regimes at 90, 75, 25, and 10 mmol photons Á m À 2 Á s À 1 accounts for negligible C growth requirements com- for more than 3 months, while receiving biweekly additions of F/2 media and prey. We were unable to grow M. rubra at pared with photosynthesis (Yih et al. 2004, Johnson À 2 À 1 and Stoecker 2005). In contrast, most kleptoplastidic 10 mmol photons Á m Á s , due to accumulation of free-liv- ing prey. This was probably due to lower ingestion and protists form recognizable food vacuoles from algal growth rates by M. rubra, and as a result, no data were avail- prey, have been shown to be capable of heterotrophy, able from this light intensity for the ciliate. All cell attribute and generally do not sequester other prey organelles and photosynthesis measurements were made on cells in mid (Lewitus et al. 1999). Because M. rubra is capable to late log phase. Prey concentrations were checked in M. rubra cultures before experimental measurements to verify of predominantly phototrophic growth and pigment À 1 synthesis, it falls into a special functional category they were at ‘‘background’’ levels (i.e. <50 cells Á mL ), while M. rubra cell concentrations during experimental meas- (Gustafson et al. 2000). urements were above 10,000 cells Á mL À 1. Experimental While many protists are thought to sequester treatments each had three replicates unless otherwise noted. chloroplasts from algal prey, relatively few studies Growth rates were estimated during the exponential portion À 1 have been conducted to evaluate plastid performance of the growth phase using m (div Á d ) 5 (log2(n1n0))t1 À t0, and function in ‘‘host’’ cells. Most studies that have where n represents cell concentrations at the beginning and evaluated carbon metabolism in kleptoplastidic protists start of the exponential growth phase. All cultures were fed about 2 weeks before experimental measurements, using have focused on oligotrich ciliates. Plastid-retaining prey acclimated to the same growth conditions. oligotrich ciliates have been shown to possess high DNA extraction, PCR amplification, and DNA sequenc- cellular photosynthetic rates (Stoecker et al. 1988), ing. Cultures of M. rubra (~3 Â 104 cells Á mL À 1)andG.cf. high plastid turnover rates (Stoecker and Silver cryophila (~1 Â 105 cells Á mL À 1) were centrifuged in 50 mL 1990), and appear to use photosynthate predomin- centrifuge tubes at 41 C and 4000g for 10 min. The Plant antly for respiration (Putt 1990). Kleptoplastidic dino- DNA Extraction Kit (Qiagen, Valencia, CA, USA) was used, flagellates, while widely documented, are less well and the manufacturer’s protocol was followed. The PCR was conducted using 1 Â PCR buffer (TaqPro, Denville, Metu- understood in regards to their physiology. Gym- chen, NJ, USA), 0.2 mM of a deoxynucleoside triphosphate nodinium gracilentum and Pfiesteria piscicida can acquire (dNTP) mixture (Bioline, Randolph, MA, USA), 0.25 mg/mL photosynthate from kleptochloroplasts for up to a BSA (Idaho Technologies, Salt Lake City, UT, USA), 3 mM week; however, the amount is insufficient to cover MgCl2 (Life Technologies, Rockville, MD, USA), 0.4 mM their entire C budget (Skovgaard 1998, Lewitus et al. primers (each), and 0.6 U Taq DNA polymerase (Denville), 1999). Recent research with M. rubra has shown that combined with 10–20 ng of genomic DNA from cultures in a volume of 25 mL. The following general eukaryotic primers plastids remain functional for up to 8 weeks in low light for SSU rRNA were used to amplify the gene from conserved (LL), while growth and pigment synthesis slowly be- regions: 4616, 4618 (Medlin et al. 1988, Oldach et al. 2000), come negligible (Johnson and Stoecker 2005). 516, and 1416 (Johnson et al. 2004). The PCR conditions In order to demonstrate that M. rubra retained plas- were as follows: an initial 3 min 951 C melting step, 40 cycles tids from Geminigera cf. cryophila (Taylor and Lee 1971, of 30 s at 951 C (melting), 30 s at 551 C (hybridization), and Hill 1991) we designed a quantitative ‘‘real-time’’ PCR 70 s at 721 C (elongation), followed by a final 10 min 721 C elongation step. Products were then cloned using a TOPO Taqman assay for the nucleomorph (Nm) small TA cloning kit (Invitrogen, Carlsbad, CA, USA), following the subunit (SSU) rRNA gene of G. cf. cryophila. The assay manufacturer’s instructions. Colonies were isolated and gene was used to quantify Nm SSU rRNA gene content by products reamplified with PCR using manufacturer supplied normalizing to G. cf. cryophila–only standards, yielding vector primers. Cloned PCR products were sequenced in an estimate of G.cf.cryophila Nm number (5plastid both directions using the above gene-specific primers and the number) per M. rubra cell. The Nm SSU rRNA gene BigDye terminator kit (Perkin Elmer, Boston, MA, USA). All was used because the Nm is always present in crypto- sequencing was conducted using an Applied Biosystems (ABI, Foster City, CA, USA) 377. Species-specific SSU phyte plastids, including those in M. rubra (Taylor et al. rDNA primers (Operon Technologies, Huntsville, AL, USA) 1969, 1971, Hibberd 1977), and the Nm SSU gene has were designed for all sequences identified from sequencing variable regions with high substitution rates and inser- the SSU rDNA clone library, and all sequences were gener- tions referred to as nonalignable regions (Hoef-Emden ated at least 10 times. et al. 2002) that allow species-specific identifications. Phylogenetic analysis. Contingent sequences were gener- Herein we contrast plastid function and performance ated using Sequencher (Gene Codes Corp., Ann Arbor, MI, USA) and added to sequences obtained from GenBank. All in the cryptophyte G.cf.cryophila with plastid function alignments were created using the Clustal X algorithm and performance in its organelle-sequestering preda- (Thompson et al.
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