Marine Ecology Progress Series 439:117

View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by ResearchOnline at James Cook University Vol. 439: 117–126, 2011 MARINE ECOLOGY PROGRESS SERIES Published October 20 doi: 10.3354/meps09315 Mar Ecol Prog Ser Symbiodinium diversity in mesophotic coral communities on the Great Barrier Reef: a first assessment Pim Bongaerts1,2,*, Eugenia M. Sampayo4, Thomas C. L. Bridge5, Tyrone Ridgway6, Francisca Vermeulen7, Norbert Englebert1, Jody M. Webster8, Ove Hoegh-Guldberg2,3 1School of Biological Sciences, 2ARC Centre of Excellence for Coral Reef Studies, and 3Global Change Institute, The University of Queensland, St Lucia, Queensland 4072, Australia 4Department of Biology, The Pennsylvania State University, University Park, Pennsylvania 16802, USA 5School of Earth and Environmental Sciences, James Cook University, Townsville, Queensland 4811, Australia 6Australian Institute of Marine Science, The UWA Oceans Institute (M096), Crawley, Western Australia 6009, Australia 7School of Biological Sciences, Victoria University of Wellington, Wellington 6140, New Zealand 8School of Geosciences, The University of Sydney, Sydney, New South Wales 2006, Australia ABSTRACT: Despite a growing interest in mesophotic coral ecosystems (MCEs), information on the photosynthetic endosymbionts (genus Symbiodinium) associated with scleractinian corals inhabiting deep reef ecosystems is sparse. Here, the deep-water Symbiodinium diversity is assessed from 10 different coral genera at a depth range of 45 to 70 m on the Great Barrier Reef (GBR), Australia. Symbiodinium identity was established using denaturing gradient gel elec- trophoresis (DGGE) fingerprinting of the internal transcribed spacer region 2 (ITS2) of the ribosomal DNA. Except for the novel Symbiodinium type C131 (found in Porites), all Symbiodinium types have previously been identified in shallow reef corals across the Pacific. Specimens of Seri- atopora, Montipora, and Porites harboured similar symbionts as reported in shallow water (e.g. C3n, C3n-hh, C15, and C17), thus adhering to patterns of host-specificity across a wide depth range. However, several other Symbiodinium types were found to transcend previously established patterns of host-specificity at mesophotic depths. For example, ‘host-specialist’ types C3i and C3k (previously only reported in Acropora spp.) were found here to associate with a range of different genera (Leptoseris, Pachyseris, Fungia, and Echinophyllia). Although limited in sample size, this preliminary survey indicates that mesophotic habitats on the GBR may not represent an isolated community in terms of Symbiodinium diversity, which has significant relevance to their potential to act as refugia. Moreover, the present study identifies the need to examine symbiont diversity across broad environmental ranges (including MCEs) in order to gain an accurate understanding of symbiosis specificity and distribution range of specific coral-Symbiodinium associations. KEY WORDS: Symbiodinium · Mesophotic · Deep reefs · Coral · ITS2 · DGGE · Great Barrier Reef Resale or republication not permitted without written consent of the publisher INTRODUCTION ans and dinoflagellates of the genus Symbiodinium (Muscatine et al. 1981). Given the important role that The successful establishment and persistence of Symbiodinium plays in the success of coral reef coral reef ecosystems in tropical nutrient-poor waters ecosystems, it is not surprising that this group has is made possible by the symbiosis between cnidari- received much attention, and the genetic characteri- *Email: [email protected] © Inter-Research 2011 · www.int-res.com 118 Mar Ecol Prog Ser 439: 117–126, 2011 zation of Symbiodinium into cladal (e.g. Rowan & connectivity (Bongaerts et al. 2010a, Frade et al. Powers 1991, Baker & Rowan 1997) and subcladal 2010) if host and symbiont lineages are coupled types (e.g. van Oppen et al. 2001, LaJeunesse 2002) through co-evolutionary processes (Loh et al. 2001, has greatly enhanced our understanding of the sym- Sampayo et al. 2007, Frade et al. 2008a). Given the biosis. Studies of Symbiodinium diversity on broad prevalence of niche specialization and ecological latitudinal or longitudinal gradients have shown zonation of Symbiodinium (LaJeunesse et al. 2003, distinct biogeographical patterns (e.g. LaJeunesse 2004, Finney et al. 2010), it is expected that extensive et al. 2003, 2010, Silverstein et al. 2011), whereas differences in Symbiodinium diversity occur be - more local or species-specific studies have high- tween shallow and deep habitats. lighted ecological zonation, physiological diversifi - Here we provide an initial assessment of Sym- cation, and host-specificity of distinct symbionts biodinium diversity associated with the mesophotic (e.g. Rowan & Knowlton 1995, LaJeunesse et al. coral communities that occur at depths ranging 2003, 2004, Iglesias-Prieto et al. 2004, Sampayo et al. from ~45 to 70 m on the Great Barrier Reef (GBR) 2007, Frade et al. 2008a). (Bridge et al. 2011a,b,c). Specimens (n = 45) col- Community-wide shifts in symbiont diversity occur lected on a research expedition (Webster et al. with increasing depth (LaJeunesse 2002, LaJeunesse 2008) were used to assess symbiont diversity from et al. 2003, 2004, 2010), but this observation is likely MCEs using denaturing gradient gel electrophore- to be, in part, the result of host community composi- sis (DGGE) fingerprinting of the internal tran- tion changes over depth. Nonetheless, studies focus- scribed spacer region 2 (ITS2) of the ribosomal ing on single coral species show a similar pattern, DNA. Symbiodinium diversity was compared to and depth zonation of symbionts has been shown to previously published information on related coral occur on a cladal level in a number of Caribbean taxa from shallower GBR locations to provide a first coral species such as Acropora cervicornis, Montas- indication of whether mesophotic corals associate traea annularis, M. franski, M. faveolata, Stephano - with a distinct deep-water Symbiodinium commu- coenia intersepta, and Porites asteroides (Rowan & nity and whether known patterns of host-symbiont Knowlton 1995, Baker et al. 1997, Toller et al. 2001, specificity are maintained across broad bathymetric Iglesias-Prieto et al. 2004, Warner et al. 2006). Sym- ranges. biont depth zonation is further observed using taxo- nomic identification at the subcladal, or ‘type’, level (LaJeunesse 2002) in species such as Madracis MATERIALS AND METHODS pharensis (Frade et al. 2008a) or Montastraea caver- nosa in the Caribbean (Warner et al. 2006), and Pocil- A total of 45 coral colonies were collected from 45 to lopora damicornis, Seriatopora hystrix, or Stylophora 70 m depth using rock dredge sampling during an pistillata in the Indo-Pacific (Sampayo et al. 2007, exploratory cruise on the RV ‘Southern Surveyor’ Bongaerts et al. 2010a). Most studies of Symbio- (September to October 2007). Samples were col lected dinium diversity have been limited to shallow waters from 3 locations (Fig. 1): (1) Ribbon Reefs (northern of less than 30 m and do not cover the full bathymet- GBR: 15° 38’ S, 145° 80’ E; 15° 49’ S, 145° 82’ E), (2) ric range of coral species (but see Lesser et al. 2010, Nog gin Pass (northern GBR: 17° 09’ S, 146° 57’ E; Cooper et al. 2011a, van Oppen et al. 2011). As a 17° 10’ S; 146° 57’ E), and (3) Hydro graphers Passage result, limited information is available on the Sym- (central GBR: 19° 69’ S. 150° 23’ E). A large fragment biodinium from mesophotic (>30 m) coral communi- of each colony was stored in 95% ethanol, and the re- ties and the extent to which these communities over- mainder was bleached and deposited at the Queens- lap with adjacent shallow water coral communities land Museum (Townsville, Australia) for further taxo- (Bongaerts et al. 2010b). nomic identification. Mesophotic coral ecosystems (MCEs) may poten- The specimen samples preserved in ethanol were tially play an important role in the overall resilience drained and the supernatant was rinsed using a of reef ecosystems by functioning as refugia during 3-fold wash step using DNAB and centrifugation at periods of stress (Glynn 1996, Hughes & Tanner 25 000 × g. DNA was extracted using a QIAGEN 2000) and representing subsequent sources of Plant Mini Kit with inclusion of all optional steps sug- propagules for recovering shallow reef habitats gested by the manufacturer. Because DNA yield of (Lesser et al. 2009, Bongaerts et al. 2010b, van Oppen some samples was low, all samples were amplified in et al. 2011). However, habitat-related differences in a nested-PCR approach (Gou et al. 2003, Hirose et al. Symbiodinium diversity may affect coral population 2008, Yamashita et al. 2010). The complete ITS Bongaerts et al.: Symbiodinium diversity in mesophotic GBR corals 119 the genera Acropora, Galaxea, and Montipora), and the nested reaction did not produce profiles different from direct amplifications. To determine the symbiont type, dominant bands were excised from 2 to 4 samples of each characteristic profile, eluted overnight in 100 µl dH2O, after which 1 µl of template Australia was used to re-amplify the DNA using the non-GC Ribbon Reefs clamped primers ITSintfor2 and ITS2reverse (cf. RR (46–70 m) LaJeunesse 2002). Successful PCR re-amplifications from excised Noggin Pass Cairns NP (54–55 m) DGGE bands were sequenced using ABI BigDye Terminator chemistry at the Australian Genome Research Facility (Brisbane, Australia). All obtained Townsville ITS2 rDNA sequences were aligned

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