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A Nanoscale Secondary Ion Mass Spectrometry Study of Dinoflagellate

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A Nanoscale Secondary Ion Mass Spectrometry Study of Dinoflagellate bs_bs_banner Environmental Microbiology (2014) doi:10.1111/1462-2920.12518 A nanoscale secondary ion mass spectrometry study of dinoflagellate functional diversity in reef-building corals Mathieu Pernice,1,2*† Simon R. Dunn,3† Linda Tonk,3 ability of the intact symbiosis between the reef- Sophie Dove,3 Isabelle Domart-Coulon,4 building coral Isopora palifera, and Symbiodinium C Peter Hoppe,5 Arno Schintlmeister,6 Michael Wagner6,7 or D types, to assimilate dissolved inorganic carbon 1,8 and Anders Meibom (via photosynthesis) and nitrogen (as ammonium). 1 Laboratory for Biological Geochemistry, School of Our results indicate that Symbiodinium types from Architecture, Civil and Environmental Engineering two clades naturally associated with I. palifera (ENAC), École Polytechnique Fédérale de Lausanne possess different metabolic capabilities. The (EPFL), Lausanne, Switzerland. Symbiodinium C type fixed and passed significantly 2 Plant Functional Biology and Climate Change Cluster more carbon and nitrogen to its coral host than the D (C3), Faculty of Science, University of Technology, type. This study provides further insights into the Sydney, NSW, Australia. metabolic plasticity among different Symbiodinium 3 ARC Centre of Excellence for Coral Reef Studies, types in hospite and strengthens the evidence that School of Biological Sciences, University of the more temperature-tolerant Symbiodinium D type Queensland, Brisbane, Qld, Australia. may be less metabolically beneficial for its coral host 4 UMR7245, Molécules de Communication et Adaptation under non-stressful conditions. des Microorganismes, Muséum National d’Histoire Naturelle, Paris, France. 5Particle Chemistry Department, Max Planck Institute for Introduction Chemistry, Mainz, Germany. 6Large-Instrument Facility for Advanced Isotope Coral reefs are among the most productive and biologically Research and 7Department of Microbiology and diverse ecosystems on Earth. The unicellular dinoflagel- Ecosystem Science, Division of Microbial Ecology, late algae (genus Symbiodinium), which live within coral University of Vienna, Vienna, Austria. tissue, play a fundamental role in the maintenance of 8Center for Advanced Surface Analysis, University of healthy reefs by providing corals with important nutrients Lausanne, Lausanne, Switzerland. (Muscatine, 1990). Thus, corals are ‘polytrophic’, being able to acquire nutrients from sunlight through their photo- synthetic symbionts (‘autotrophy’), feeding on plankton Summary (‘heterotrophy’) and absorbing dissolved nutrients from the Nutritional interactions between corals and symbiotic surrounding seawater. These multiple strategies increase dinoflagellate algae lie at the heart of the structural the nutritional options for corals in the oligotrophic environ- foundation of coral reefs. Whilst the genetic diversity ment they commonly inhabit. of Symbiodinium has attracted particular interest Symbiotic dinoflagellates of the genus Symbiodinium because of its contribution to the sensitivity of corals are divided into nine broad genetic clades, (clades A–I) to environmental changes and bleaching (i.e. disrup- defined by rRNA gene sequences (Rowan and Powers, tion of coral–dinoflagellate symbiosis), very little is 1991a; Coffroth and Santos, 2005; Pochon and Gates, known about the in hospite metabolic capabilities of 2010). These clades contain various genetically distinct different Symbiodinium types. Using a combination of types according to comparative analyses of internal tran- stable isotopic labelling and nanoscale secondary ion scribed spacer (ITS) sequence regions (van Oppen et al., mass spectrometry (NanoSIMS), we investigated the 2001; LaJeunesse et al., 2004a,b; Pochon et al., 2007; Sampayo et al., 2007). Corals can simultaneously harbour dinoflagellates from different types in variable densities depending on coral species and environmental Received 8 August, 2013; accepted 25 May, 2014. *For correspond- ence. E-mail [email protected]; Tel. +6129514 4038; Fax conditions (Baker and Romanski, 2007). Differences in +6129514 4079. †These authors contributed equally to this work. physiological properties between Symbiodinium types © 2014 Society for Applied Microbiology and John Wiley & Sons Ltd 2 M. Pernice et al. can influence photosynthetic efficiency, growth and 2013). Here, we use isotopic labelling in combination thermal tolerance of the host (Iglesias-Prieto et al., 2004; with single-cell NanoSIMS imaging of the intact coral Little et al., 2004; Berkelmans and van Oppen, 2006; symbiosis to offer an integrated view of the differential Sampayo et al., 2008). Although considered as a key ability of Symbiodinium types from different clades to factor that defines the health of coral reefs in a changing acquire dissolved inorganic carbon and nitrogen. climate, the functional diversity of most Symbiodinium In this study, we investigated (i) whether different types remains under-explored. Symbiodinium types that naturally associate with a single Assimilation of carbon and nitrogen is essential for coral species possess different metabolic capabilities and corals, and therefore, adequate supply of these two nutri- (ii) to what extent these genetically distinct symbiont types ents is critical to sustain optimal growth, development affect coral host metabolism. To address these questions, and response to a wide array of stresses. As yet, we compared the assimilation of dissolved inorganic however, most nutritional investigations of the functional carbon and nitrogen between colonies of the reef-building diversity of symbiotic dinoflagellates have focused on the coral Isopora palifera (Wallace et al., 2012) (Fig. 1A), metabolism of photosynthetically fixed carbon (Loram which associates with Symbiodinium types from clades C et al., 2007; Stat et al., 2008). Recently Baker and and D in its natural habitat. colleagues (2013) compared nitrate assimilation in juve- nile corals infected with different Symbiodinium clades Results and discussion and suggested that under non-stressful conditions, Symbiodinium type C1 outcompetes an undefined D type Sixty-eight adult I. palifera colonies growing at different via enhanced nitrogen acquisition. Nevertheless, assimi- sites adjacent to Heron Island Research Station (HIRS, lation of ammonium, which is the preferred source of 231330S 1511540E) were assessed regarding the diver- inorganic dissolved nitrogen for coral dinoflagellates sity of Symbiodinium before November 2011, when corals (Grover et al., 2008), has so far never been compared were sampled for the labelling experiment. For each between Symbiodinium types from different clades. Fur- colony, Symbiodinium clades were identified by extracting thermore, most bulk isotope analysis studies measuring genomic DNA from a single branch and analysing the the relative assimilation of carbon and nitrogen by sym- pattern of PCR-restriction fragment length polymorphism biotic dinoflagellates suffer from potential cross- (PCR-RFLP) of the small subunit rRNA gene. Fifty-nine contamination of coral host and dinoflagellate fractions, I. palifera colonies harboured Symbiodinium clade C, as the intertwined nature of the coral–dinoflagellate while eight colonies were associated with Symbiodinium endosymbiosis makes the relative quantification of dino- clade D, and only one colony hosted members of both flagellate symbiont metabolism in hospite extremely dif- clades C and D. All Symbiodinium could be further ficult (Yellowlees et al., 2008). In this context, recent assigned to either type C3 or D1 by polymorphism screen- advances in nanoscale secondary ion mass spectrom- ing of the ITS1–ITS2 region using denaturing gradient gel etry (NanoSIMS) have the potential to provide direct electrophoresis (DGGE, Fig. 1B) and sequencing of imaging and precise quantification at the individual cell excised bands (data not shown). level of up to seven different isotopes or molecular Subsequently, a combination of isotopic labelling with species within an intact symbiosis (Musat et al., 2008; 15N-ammonium and 13C-bicarbonate and NanoSIMS Pernice et al., 2012; Berry et al., 2013; Kopp et al., 2013) imaging of tissue sections was used to quantify the (for review, see Orphan and House, 2009; Hoppe et al., assimilation of dissolved inorganic carbon and nitrogen in Fig. 1. NanoSIMS quantification of 15N and 13C assimilation by two different Symbiodinium types naturally associated with the reef-building coral Isopora palifera. A. A colony of I. palifera collected on Heron Island in November 2011. B. Symbiodinium types were identified in 68 coral samples by amplification of the ITS1-ITS2 region followed by screening of polymorphisms using denaturing gradient gel electrophoresis (DGGE). In this panel DGGE data for four representative coral colonies are depicted. Selected 15 13 corals containing the different Symbiodinium types (C3 or D1) were incubated in ASW containing NH4Cl (5 μM) and NaH CO3 (2 mM) for 48 h. D–I. The distribution of 15N/14N and 13C/12C isotopic ratio was imaged directly in the coral tissue and quantified using NanoSIMS. The Hue Saturation Intensity images are mapping the 15N/14N (D, F, H) and 13C/12C (E, G, I) isotopic ratio. The rainbow scale corresponds to the isotopic ratios and ranges from blue, set to natural ratio (0.0037 for 15N/14N and 0.0110 for 13C/12C), to red, where the ratio is several fold above natural ratio (0.0370, 10 times the natural ratio for 15N/14N and 0.1100, 10 times the natural ratio for 13C/12C). Quantification of 15N and 13C enrichment of individual dinoflagellate
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