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Full Text in Pdf Format Vol. 462: 1–7, 2012 MARINE ECOLOGY PROGRESS SERIES Published August 21 doi: 10.3354/meps09914 Mar Ecol Prog Ser OPENPEN ACCESSCCESS FEATURE ARTICLE Symbiodinium spp. in colonies of eastern Pacific Pocillopora spp. are highly stable despite the prevalence of low-abundance background populations Michael P. McGinley1,*, Matthew D. Aschaffenburg1, Daniel T. Pettay1, Robin T. Smith2, Todd C. LaJeunesse3, Mark E. Warner1 1College of Earth, Ocean, and Environment, University of Delaware, Lewes, Delaware 19958, USA 2Department of Biology, Florida International University, Miami, Florida 33199, USA 3Department of Biology, The Pennsylvania State University, University Park, Pennsylvania 16802, USA ABSTRACT: A shift in the dominant Symbiodinium species within a coral colony may allow rapid ac - climatization to environmental stress, provided that the new symbiont is better suited to prevailing conditions. In this study, the Symbiodinium diver- sity in Pocillopora corals was examined following a cold-water bleaching event in the Gulf of Cali- fornia. Individual colonies were differentially im - pacted by this event based upon their association with either the Symbiodinium ITS-2 type C1b-c (sensitive) or ITS-2 type D1 (tolerant). Real-time PCR indicated a high prevalence of an alternate and compatible Symbiodinium sp. (i.e. C1b-c or D1) residing at low-abundance background levels within many colonies both during and after a 1 yr recovery interval (46 to 52%). However, despite the potential for ‘switching,’ the dominant resident symbiont remained at high abundance during the Resident Symbiodinium spp. remained stable within Pocillo- recovery, with only 2 of 67 colonies (3%) under - pora corals following a cold-water stress event off Baja going a change to the other Symbiodinium type. Cali fornia, Mexico, in 2008. Pocillopora residing in the Gulf of California there- Photos: T.C. LaJeunesse, M. D. Aschaffenburg, D.T. Pettay fore maintain long-term associations dominated by a specific Symbiodinium sp., where potential com- petition by a second symbiont type is suppressed INTRODUCTION despite the temporary change in environmental conditions that would favor a shift in symbiosis The survival of a coral colony is dependent on the toward a more stress-tolerant species. physiological limitations of both the cnidarian host KEY WORDS: Coral bleaching · Real-time PCR · and its endosymbiotic dinoflagellate (Symbiodinium Symbiodinium · Symbiosis · Pocillopora · Eastern spp.) under prevailing environmental conditions Pacific (Iglesias-Prieto & Trench 1997). The physiological contribution of each partner determines the level of Resale or republication not permitted without written consent of the publisher sensitivity or resiliency of a coral to environmental *Email: [email protected] © Inter-Research 2012 · www.int-res.com 2 Mar Ecol Prog Ser 462: 1–7, 2012 stress (Brown et al. 2002, Rowan 2004, Berkelmans & ing in the southern Gulf of California, in which corals van Oppen 2006, Baird et al. 2009, Wicks et al. 2012). harboring the sensitive symbiont, Symbiodinium When grown under identical conditions, genetically ITS-2 type C1b-c, were severely bleached, while the distinct isolates of Symbiodinium exhibit consider- colonies associated with Symbiodinium ITS-2 type able differences in their ability to acclimatize to both D1 were largely unaffected (LaJeunesse et al. light (Iglesias-Prieto & Trench 1997, Reynolds et al. 2010a). The present study compared the temporal 2008, Hennige et al. 2009) and temperature stress stability of these Symbiodinium communities within (Berkelmans & van Oppen 2006, Robison & Warner Pocillopora spp. at the end of the bleaching event 2006), both of which are important factors responsi- (May 2008) and following a 1 yr recovery interval ble for large-scale coral bleaching events (Fitt et al. (June 2009) using real-time PCR. This sensitive de - 2001). Therefore, the physiological attributes of a tection technique confirmed that despite the poten- coral’s symbiont are important factors determining tial for populations of D1 symbionts to proliferate and the persistence of coral communities subjected to acute outcompete type C1b-c symbionts, the dominant and long-term changes in their resident environment symbiont remained remarkably stable during recov- (Sampayo et al. 2008, LaJeunesse et al. 2010a). ery for the majority of colonies. If corals continue to survive under the current rate of climate change (IPCC 2007), one mechanism for rapid physiological change could involve a shift in MATERIALS AND METHODS coral symbioses to Symbiodinium spp. better adapted to more stressful environmental conditions (e.g. All experimental coral fragments were obtained higher temperatures; Baker 2001). Therefore, severe from Punta Galeras Reef, Gulf of California physiological stress and disruption of the normal (24° 21’ 15’’ N, 110° 17’ 05’’ W), near La Paz, Mexico. symbiosis (i.e. bleaching) may present an opportu- In May 2008, fragments (~4 to 5 cm in size) from 77 nity for rapid acclimatization by allowing for the pro- distinct parent colonies of Pocillopora spp. were sam- liferation of a tolerant background symbiont popu - pled following a cold-water bleaching event, caused lation, a condition known as symbiont ‘shuffling’ by an unusually strong La Niña cycle in this region (Rowan et al. 1997, Berkelmans & van Oppen 2006, (see LaJeunesse et al. 2010a), based on the visual Jones et al. 2008, LaJeunesse et al. 2009). A coral characterization of bleached (completely white colony; species capable of associating with several symbiotic n = 43) or non-bleached (brown colony; n = 34). This partners could possess an ecological advantage in visual characterization of bleaching was confirmed its ability to adjust to different stressors imposed by by symbiont isolation and quantification, such that global climate change. bleached colonies contained significantly fewer sym- Although most corals appear to develop highly bionts relative to coral fragments sampled 1 yr prior specific and stable associations with particular algal to the bleaching event at this same location in 2007, partners (Goulet 2006), the recent use of increasingly while there was no significant change in symbiont sensitive molecular techniques (i.e. real-time PCR) number for the same comparison in non-bleached have detected low-level, background symbiont pop- fragments (LaJeunesse et al. 2010a). Initially, a frag- ulations that belong to a clade group different from ment from each colony was analyzed for its original the typical dominant symbiont (Loram et al. 2007, Symbiodinium composition (see below), mounted Mieog et al. 2007, Correa et al. 2009, Silverstein et al. with marine epoxy to a labeled 1.5 inch PVC pipe 2012). These findings were used to infer that the coupler, and transplanted back to the reef site for a potential of symbiont shuffling is higher than previ- 1 yr recovery interval. In June 2009, all previously ously thought. However, in only a few cases has it transplanted colony fragments were collected and been shown that background symbiont populations again sampled for the genetic analysis of their Sym- may be ecologically important during episodes of in - biodinium. Ten of the colonies (2 C1b-c and 8 D1 creasing stress (e.g. Berkelmans & van Oppen 2006, corals) were excluded from our analysis due to mor- LaJeunesse et al. 2009). Understanding the flexibility tality or problems with extracting quality DNA (n = of different coral-algal symbioses, as well as the eco- 67 remaining colonies). logical role of background symbionts, is crucial to Small fragments were removed from each coral fully comprehending the biological impact that cli- using bone cutters and preserved in a high salt 20% mate change will have on coral communities. DMSO DNA preservation buffer prior to transport In 2008, an anomalous cold-water bleaching event back to the USA (Seutin et al. 1991). A Wizard DNA differentially impacted colonies of Pocillopora resid- extraction protocol (Promega) was applied using McGinley et al.: Stability in Pocillopora-Symbiodinium associations 3 1.0 mm glass beads to homogenize the tissue from The DNA samples used to construct each dilution each fragment. The genetic identity of the Symbio- were extracted from pelleted Symbiodinium cells dinium sp. was initially examined using PCR-dena- (isolated from the host or a culture [B1] via centrifu- turing gradient gel electrophoresis (DGGE) of the gation) and screened by real-time PCR to ensure the ITS2 rDNA to characterize the dominant Symbio- absence of any background symbionts. The conserv- dinium sp. as either C1b-c or D1 (LaJeunesse et al. ative cutoff point represents the highest CT values at 2008). All samples were amplified using the ‘ITS2 which the dilution series remained linear (CT versus Clamp’ and ‘ITSintfor2’ using a touchdown PCR pro- log scale concentration), with a standard deviation of tocol according to LaJeunesse (2002). The resulting <0.25 among the technical replicates. PCR products were electrophoresed on an 8% poly- The resulting CT values for the C and D primer sets acrylamide denaturing gradient gel (45 to 80% were used to designate each sample into one of denaturant) for 16 h at 115 V (CBScientific System). the following categories: C1b-c or D1 only (a single The samples were additionally analyzed using pre- clade detected), C1b-c/D1 mixture (<3 CT difference viously developed Clade B, C, and D specific real- between clades), C1b-c dominated with a D1 in time PCR primers designed to target differences
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