Variation in Symbiodinium ITS2 Sequence Assemblages among Coral Colonies

et al. (2011) Variation in Symbiodinium ITS2 Sequence Assemblages among Coral Colonies. PLoS ONE 6(1): e15854. doi:10.1371/journal.pone.0015854 Variation in Symbiodinium ITS2 Sequence Assemblages among Coral Colonies Michael Stat 0 Christopher E. Bird 0 Xavier Pochon 0 Luis Chasqui 0 Leonard J. Chauka 0 Gregory T. Concepcion 0 Dan Logan 0 Misaki Takabayashi 0 Robert J. Toonen 0 Ruth D. Gates 0 Dirk Steinke, Biodiversity Insitute of Ontario - University of Guelph, Canada 0 1 Hawai'i Institute of Marine Biology, School of Ocean and Earth Science and Technology, University of Hawai'i, Ka ne'ohe, Hawai'i, United States of America, 2 Instituto de Investigaciones Marinas y Costeras ''Jose Benito Vives de Andre is'' INVEMAR. A.A., Santa Marta, Colombia, 3 Institute of Marine Sciences, University of Dar es Salaam, Zanzibar, Tanzania, 4 School of Biological Sciences, Victoria University of Wellington , Wellington , New Zealand , 5 Department of Marine Science, University of Hawai'i at Hilo , Hilo, Hawai'i , United States of America Endosymbiotic dinoflagellates in the genus Symbiodinium are fundamentally important to the biology of scleractinian corals, as well as to a variety of other marine organisms. The genus Symbiodinium is genetically and functionally diverse and the taxonomic nature of the union between Symbiodinium and corals is implicated as a key trait determining the environmental tolerance of the symbiosis. Surprisingly, the question of how Symbiodinium diversity partitions within a species across spatial scales of meters to kilometers has received little attention, but is important to understanding the intrinsic biological scope of a given coral population and adaptations to the local environment. Here we address this gap by describing the Symbiodinium ITS2 sequence assemblages recovered from colonies of the reef building coral Montipora capitata sampled across Kane'ohe Bay, Hawai'i. A total of 52 corals were sampled in a nested design of Coral Colony(Site(Region)) reflecting spatial scales of meters to kilometers. A diversity of Symbiodinium ITS2 sequences was recovered with the majority of variance partitioning at the level of the Coral Colony. To confirm this result, the Symbiodinium ITS2 sequence diversity in six M. capitata colonies were analyzed in much greater depth with 35 to 55 clones per colony. The ITS2 sequences and quantitative composition recovered from these colonies varied significantly, indicating that each coral hosted a different assemblage of Symbiodinium. The diversity of Symbiodinium ITS2 sequence assemblages retrieved from individual colonies of M. capitata here highlights the problems inherent in interpreting multi-copy and intra-genomically variable molecular markers, and serves as a context for discussing the utility and biological relevance of assigning species names based on Symbiodinium ITS2 genotyping. - Funding: This research was funded by the Edwin Pauley Foundation; the Global Environment Facility-World Bank Coral Reef Targeted Research Project (www. gefcoral.org); the National Science Foundation (OCE-0752604 to RDG and OIA-0554657 administered by University of Hawaii), the Swiss National Science Foundation (PBGEA-115118 to XP), and University of Hawaii Sea Grant College Program (Project #R/CR-16 NA050AR4171048 to MT). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing Interests: The authors have declared that no competing interests exist. Coral reefs are biologically diverse ecosystems providing habitat for a wide range of marine organisms. The growth of corals and their ability to form the calcium carbonate substrate reflects their endosymbioses with photosynthetic dinoflagellates belonging to the genus Symbiodinium [1]. Nine divergent lineages, clades AI, have been described in Symbiodinium based on nuclear ribosomal DNA (rDNA) and chloroplast 23S rDNA [2] with each clade containing multiple genetic varieties often resolved using the internal transcribed spacer (ITS) regions [e.g. 36]. Symbiodinium diversity is partitioned by a variety of factors including biogeographical barriers, host species, colony depth, irradiance, and host symbiont transmission strategy [710]. Biogeographic patterns in Symbiodinium are evident between reefs in different oceans (Pacific versus Atlantic) [9], among reefs within an ocean (e.g. Pacific reefs in Japan and the Great Barrier Reef Australia) [11,12], and from reefs across a latitudinal gradient (e.g. eastern Australia coastline) [12,13]. The same coral species from inshore and offshore reefs within the same reef complex (e.g. in the central Great Barrier Reef or in Panama) can also associate with different Symbiodinium [12,14], as can colonies of the same species from the same reef environment [5,10,14,15]. Fidelity in the association between some coral species and Symbiodinium has lead to a degree of co-evolution resulting in host-symbiont specificity [9,16]. For example, the ITS2 Symbiodinium genotype C42 associates with Pocillopora and C31 with Montipora [9]. Attributed to levels of irradiation, Symbiodinium in corals such as Montastraea spp. and Madracis pharensis in Panama [8,17] and Pocillopora damicornis in the Great Barrier Reef [18] partition as a function of depth and/or location on individual colonies [8]. Host symbiont acquisition strategy also affects Symbiodinium assemblages with hosts that acquire their symbionts from the environment (horizontal symbiont acquisition strategy) primarily associating with a similar pool of symbionts, and those that acquire their symbionts from the parent colony (vertical symbiont acquisition strategy) harboring their own unique suite of symbionts specific to a host genus [9,10]. Understanding the factors that affect distribution and specificity patterns in coral-dinoflagellate symbioses and the physiological range of host-symbiont combinations is important for understanding how corals will respond to environmental change. In this regard, functional variability in isolated Symbiodinium types and specific coral-Symbiodinium symbioses have been correlated with numerous factors. Variation in the photophysiology of Symbiodinium [17,19,20], growth rate of coral colonies [21], symbiont carbon fixation and translocation to the host [22,23], symbiont thermal tolerance [24], and host disease susceptibility [22] all provide evidence for range thresholds in physiological performance of different host-symbiont assemblages as a response to the environment. As coral bleaching and disease are predicted to impact coral reef ecosystems in the future and have recently increased in severity and occurrence [25,26], the different hostsymbiont combinations that can occur and the environmental tolerance of those symbioses will provide the framework for predicting future shifts in coral reef communities. The number of unique Symbiodinium that reside in individual coral hosts is an (...truncated)