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Todd C Lajeunesse - One of the best experts on this subject based on the ideXlab platform.

  • validation and description of Symbiodinium microadriaticum the type species of Symbiodinium dinophyta
    Journal of Phycology, 2017
    Co-Authors: Todd C Lajeunesse
    Abstract:

    It has been 55 years since Hugo Freudenthal described Symbiodinium microadriaticum (Dinophyceae), the type species of this large and important dinoflagellate genus found commonly in mutualistic symbiosis with cnidarians, other invertebrates, and certain protists. However, no type specimen was designated by Freudenthal, thus S. microadriaticum was invalid, as was Symbiodinium and every species subsequently assigned to the genus. The original culture was lost, but since 1979, a different culture, CCMP2464/rt-061, had been considered to represent S. microadriaticum. From this culture, a preserved specimen is herein designated the holotype of S. microadriaticum, validating the binomial and Symbiodinium. All binary designations previously considered to belong in Symbiodinium also are validated herein.

  • Symbiodinium glynnii sp nov a species of stress tolerant symbiotic dinoflagellates from pocilloporid and montiporid corals in the pacific ocean
    Phycologia, 2017
    Co-Authors: Drew C Wham, Gang Ning, Todd C Lajeunesse
    Abstract:

    Abstract A formal Symbiodinium species taxonomy enhances understanding of the physiology and ecology of coral–dinoflagellate symbioses. Here we formally define a new species of stress tolerant Symbiodinium in Clade D, Symbiodinium glynnii sp. nov. This species exhibits high host specificity for members of the stony coral genus Pocillopora in the Pacific Ocean and can also be found in symbiosis with the coral genera Seriatopora and Montipora. Symbiodinium glynnii is especially common in the Eastern Tropical and subtropical Pacific, where Pocillopora is abundant and ecologically important. While S. glynnii is evolutionarily closely related to Symbiodinium trenchii, a combination of multilocus genetic data including rDNA, chloroplast (psbA), and single copy nuclear microsatellites, as well as differences in ecology (host associations), morphology (cell size), and ultrastructure (chromosome size), identify S. glynnii as distinct from S. trenchii and other Clade D species. Finally we use these data to paramete...

  • biogeography and molecular diversity of coral symbionts in the genus Symbiodinium around the arabian peninsula
    Journal of Biogeography, 2017
    Co-Authors: Maren Ziegler, Cornelia Roder, Chatchanit Arif, Todd C Lajeunesse, John A Burt, Sergey Dobretsov, Christian R. Voolstra
    Abstract:

    Aim Coral reefs rely on the symbiosis between scleractinian corals and intracellular, photosynthetic dinoflagellates of the genus Symbiodinium making the assessment of symbiont diversity critical to our understanding of ecological resilience of these ecosystems. This study characterizes Symbiodinium diversity around the Arabian Peninsula, which contains some of the most thermally diverse and understudied reefs on Earth. Location Shallow water coral reefs throughout the Red Sea (RS), Sea of Oman (SO), and Persian/Arabian Gulf (PAG). Methods Next-generation sequencing of the ITS2 marker gene was used to assess Symbiodinium community composition and diversity comprising 892 samples from 46 hard and soft coral genera. Results Corals were associated with a large diversity of Symbiodinium, which usually consisted of one or two prevalent symbiont types and many types at low abundance. Symbiodinium communities were strongly structured according to geographical region and to a lesser extent by coral host identity. Overall symbiont communities were composed primarily of species from clade A and C in the RS, clade A, C, and D in the SO, and clade C and D in the PAG, representing a gradual shift from C- to D-dominated coral hosts. The analysis of symbiont diversity in an Operational Taxonomic Unit (OTU)-based framework allowed the identification of differences in symbiont taxon richness over geographical regions and host genera. Main conclusions Our study represents a comprehensive overview over biogeography and molecular diversity of Symbiodinium in the Arabian Seas, where coral reefs thrive in one of the most extreme environmental settings on the planet. As such our data will serve as a baseline for further exploration into the effects of environmental change on host–symbiont pairings and the identification and ecological significance of Symbiodinium types from regions already experiencing ‘Future Ocean’ conditions.

  • most low abundance background Symbiodinium spp are transitory and have minimal functional significance for symbiotic corals
    Microbial Ecology, 2016
    Co-Authors: Moo Joon Lee, Hae Jin Jeong, Nam Seon Kang, Drew C Wham, Se Hyeon Jang, Sung Yeon Lee, Kyung Ha Lee, Hyung Seop Kim, Todd C Lajeunesse
    Abstract:

    Speculation surrounds the importance of ecologically cryptic Symbiodinium spp. (dinoflagellates) that occur at low abundances in reef-building corals and in the surrounding environment. Evidence acquired from extensive sampling, long-term monitoring, and experimental manipulation can allow us to deduce the ecology and functional significance of these populations and whether they might contribute to the response of coral-dinoflagellate mutualisms to climate change. Quantitative PCR was used here to diagnose the prevalence, seasonal variation, and abundances of Symbiodinium spp. within and between colonies of the coral, Alveopora japonica. Consistent with broader geographic sampling, only one species comprised 99.9 %, or greater, the population of symbionts in every sample. However, other Symbiodinium including the non-mutualistic species, Symbiodinium voratum, were often detected, but at estimated cell densities thousands-fold less than the dominant symbiont. The temporal variation in prevalence and abundances of these "background" Symbiodinium could not be definitively related to any particular environmental factor including seasonality and water chemistry. The prevalence (proportion detected among host samples), but not abundance, of S. voratum may weakly correspond to increases in environmental inorganic silica (SiO2) and possibly nitrogen (NO3). When multiple background Symbiodinium occurred within an individual polyp, the average cell densities were positively correlated, suggesting non-specific processes of cell sorting and retention by the animal. While these findings substantiate the existence of a broader, yet uncharacterized, diversity of Symbiodinium, we conclude that only those species which can occur in high abundance and are temporally stable are ultimately important to coral-dinoflagellate mutualisms. Many transient Symbiodinium spp., which occur only at trace abundances in the coral's microbiome, belong to different functional guilds and likely have little, if any, importance to a coral's physiology. The successful integration between host and symbiont into a stable functional unit should therefore be considered when defining host-symbiont specificity.

  • Symbiodinium tridacnidorum sp nov a dinoflagellate common to indo pacific giant clams and a revised morphological description of Symbiodinium microadriaticum freudenthal emended trench blank
    European Journal of Phycology, 2015
    Co-Authors: Sung Yeon Lee, Hae Jin Jeong, Nam Seon Kang, Se Hyeon Jang, Tae Young Jang, Todd C Lajeunesse
    Abstract:

    ABSTRACTThe dinoflagellate genus Symbiodinium contains numerous genetically distinct lineages that appear ‘morphologically cryptic’. However, detailed morphological assessments of plate formulae visible in the motile phase (mastigote) of two distantly related Symbiodinium spp., representing Clades ‘A’ and ‘E’, were recently shown to be different. While there are several formally described species in Clade A, genetic evidence indicates that many more remain uncharacterized. We focused on closely related phylogenetic lineages within this group to examine whether differences in morphology can be used together with genetic and ecological evidence to describe new species. We found fixed differences in nuclear (internal transcribed spacer (ITS) and large subunit rDNA), chloroplast (cp23S) and mitochondrial (cob) gene sequences from cultured and field-collected samples of Symbiodinium microadriaticum (sensu Trench & Blank, 1987) and Symbiodinium sp. associated predominantly with giant clams and Pacific Cassiopea...

Ruth D. Gates - One of the best experts on this subject based on the ideXlab platform.

  • Variability of Symbiodinium Communities in Waters, Sediments, and Corals of Thermally Distinct Reef Pools in American Samoa
    2016
    Co-Authors: Ross Cunning, Hollie M. Putnam, Denise M. Yost, Marisa L. Guarinello, Ruth D. Gates
    Abstract:

    Reef-building corals host assemblages of symbiotic algae (Symbiodinium spp.) whose diversity and abundance may fluctuate under different conditions, potentially facilitating acclimatization to environmental change. The composition of free-living Symbiodinium in reef waters and sediments may also be environmentally labile and may influence symbiotic assemblages by mediating supply and dispersal. The magnitude and spatial scales of environmental influence over Symbiodinium composition in different reef habitat compartments are, however, not well understood. We used pyrosequencing to compare Symbiodinium in sediments, water, and ten coral species between two backreef pools in American Samoa with contrasting thermal environments. We found distinct compartmental assemblages of clades A, C, D, F, and/or G Symbiodinium types, with strong differences between pools in water, sediments, and two coral species. In the pool with higher and more variable temperatures, abundance of various clade A and C types differed compared to the other pool, while abundance of D types was lower in sediments but higher in water and in Pavona venosa, revealing an altered habitat distribution and potential linkages among compartments. The lack of between-pool effects in other coral species was due to either low overall variability (in the case of Porites) or high within-pool variability. Symbiodinium communities in water and sediment also showed within-pool structure, indicating that environmental influences may operate over multiple, small spatial scales. This work suggests that Symbiodinium composition is highly labile in reef waters, sediments, and some corals, but the underlying drivers and functional consequences of this plasticity require further testing with high spatial resolution biological and environmental sampling.

  • Multi-gene analysis of Symbiodinium dinoflagellates: a perspective on rarity, symbiosis, and evolution.
    PeerJ, 2014
    Co-Authors: Xavier Pochon, Hollie M. Putnam, Ruth D. Gates
    Abstract:

    Symbiodinium, a large group of dinoflagellates, live in symbiosis with marine protists, invertebrate metazoans, and free-living in the environment. Symbiodinium are functionally variable and play critical energetic roles in symbiosis. Our knowledge of Symbiodinium has been historically constrained by the limited number of molecular markers available to study evolution in the genus. Here we compare six functional genes, representing three cellular compartments, in the nine known Symbiodinium lineages. Despite striking similarities among the single gene phylogenies from distinct organelles, none were evolutionarily identical. A fully concatenated reconstruction, however, yielded a well-resolved topology identical to the current benchmark nr28S gene. Evolutionary rates differed among cellular compartments and clades, a pattern largely driven by higher rates of evolution in the chloroplast genes of Symbiodinium clades D2 and I. The rapid rates of evolution observed amongst these relatively uncommon Symbiodinium lineages in the functionally critical chloroplast may translate into potential innovation for the symbiosis. The multi-gene analysis highlights the potential power of assessing genome-wide evolutionary patterns using recent advances in sequencing technology and emphasizes the importance of integrating ecological data with more comprehensive sampling of free-living and symbiotic Symbiodinium in assessing the evolutionary adaptation of this enigmatic dinoflagellate.

  • the distribution of the thermally tolerant symbiont lineage Symbiodinium clade d in corals from hawaii correlations with host and the history of ocean thermal stress
    Ecology and Evolution, 2013
    Co-Authors: Michael Stat, Xavier Pochon, Erik C Franklin, John F Bruno, Kenneth S Casey, Elizabeth R Selig, Ruth D. Gates
    Abstract:

    Spatially intimate symbioses, such as those between scleractinian corals and unicellular algae belonging to the genus Symbiodinium, can potentially adapt to changes in the environment by altering the taxonomic composition of their endosymbiont communities. We quantified the spatial relationship between the cumulative frequency of thermal stress anomalies (TSAs) and the taxonomic composition of Symbiodinium in the corals Montipora capitata, Porites lobata, and Porites compressa across the Hawaiian archipelago. Specifically, we investigated whether thermally tolerant clade D Symbiodinium was in greater abundance in corals from sites with high frequencies of TSAs. We recovered 2305 Symbiodinium ITS2 sequences from 242 coral colonies in lagoonal reef habitats at Pearl and Hermes Atoll, French Frigate Shoals, and Kaneohe Bay, Oahu in 2007. Sequences were grouped into 26 operational taxonomic units (OTUs) with 12 OTUs associated with Montipora and 21 with Porites. Both coral genera associated with Symbiodinium in clade C, and these co-occurred with clade D in M. capitata and clade G in P. lobata. The latter represents the first report of clade G Symbiodinium in P. lobata. In M. capitata (but not Porites spp.), there was a significant correlation between the presence of Symbiodinium in clade D and a thermal history characterized by high cumulative frequency of TSAs. The endogenous community composition of Symbiodinium and an association with clade D symbionts after long-term thermal disturbance appear strongly dependent on the taxa of the coral host.

  • genetic diversity of free living Symbiodinium in surface water and sediment of hawai i and florida
    Coral Reefs, 2012
    Co-Authors: Misaki Takabayashi, Xavier Pochon, L M Adams, Ruth D. Gates
    Abstract:

    Marine dinoflagellates in the genus Symbiodinium are primarily known for their symbiotic associations with invertebrates and protists, although they are also found free-living in nanoplankton and microphytobenthic communities. Free-living Symbiodinium are necessary for hosts that must acquire their symbionts anew each generation and for the possible reestablishment of endosymbiosis in bleached adults. The diversity and ecology of free-living Symbiodinium are not well studied by comparison with their endosymbiotic counterparts, and as a result, our understanding of the linkages between free-living and endosymbiotic Symbiodinium is poor. Here, we begin to address this knowledge gap by describing the genetic diversity of Symbiodinium in the surface water and reef sediments of Hawai‘i and Florida using Symbiodinium-specific primers for the hypervariable region of the chloroplast 23S domain V (cp23S-HVR). In total, 29 Symbiodinium sequence types were detected, 16 of which were novel. The majority of Symbiodinium sequence types in free-living environments belonged to clades A and B, but smaller numbers of sequence types belonging to clades C, D, and G were also detected. The majority of sequences recovered from Hawai‘i belonged to clades A and C and those from Florida to clade B. Such distribution patterns are consistent with the endosymbiotic diversity previously reported for these two regions. The ancestral sequence types in each clade were typically recovered from surface water and sediments both in Hawai‘i and Florida and have been previously reported as endosymbionts of a range of invertebrates, suggesting that these types have the capacity to exploit a range of very different habitats. More derived sequence types in clades A, B, C, and G were not recovered here, suggesting they are potentially restricted to endosymbiotic environments.

  • identifying and characterizing alternative molecular markers for the symbiotic and free living dinoflagellate genus Symbiodinium
    PLOS ONE, 2012
    Co-Authors: Xavier Pochon, Hollie M. Putnam, Fabien Burki, Ruth D. Gates
    Abstract:

    Dinoflagellates in the genus Symbiodinium are best known as endosymbionts of corals and other invertebrate as well as protist hosts, but also exist free-living in coastal environments. Despite their importance in marine ecosystems, less than 10 loci have been used to explore phylogenetic relationships in this group, and only the multi-copy nuclear ribosomal Internal Transcribed Spacer (ITS) regions 1 and 2 have been used to characterize fine-scale genetic diversity within the nine clades (A–I) that comprise the genus. Here, we describe a three-step molecular approach focused on 1) identifying new candidate genes for phylogenetic analysis of Symbiodinium spp., 2) characterizing the phylogenetic relationship of these candidate genes from DNA samples spanning eight Symbiodinium clades (A–H), and 3) conducting in-depth phylogenetic analyses of candidate genes displaying genetic divergences equal or higher than those within the ITS-2 of Symbiodinium clade C. To this end, we used bioinformatics tools and reciprocal comparisons to identify homologous genes from 55,551 cDNA sequences representing two Symbiodinium and six additional dinoflagellate EST libraries. Of the 84 candidate genes identified, 7 Symbiodinium genes (elf2, coI, coIII, cob, calmodulin, rad24, and actin) were characterized by sequencing 23 DNA samples spanning eight Symbiodinium clades (A–H). Four genes displaying higher rates of genetic divergences than ITS-2 within clade C were selected for in-depth phylogenetic analyses, which revealed that calmodulin has limited taxonomic utility but that coI, rad24, and actin behave predictably with respect to Symbiodinium lineage C and are potential candidates as new markers for this group. The approach for targeting candidate genes described here can serve as a model for future studies aimed at identifying and testing new phylogenetically informative genes for taxa where transcriptomic and genomics data are available.

Ove Hoeghguldberg - One of the best experts on this subject based on the ideXlab platform.

  • Symbiodinium dinophyceae community patterns in invertebrate hosts from inshore marginal reefs of the southern great barrier reef australia
    Journal of Phycology, 2017
    Co-Authors: Linda Tonk, Eugenia M Sampayo, Aaron Chai, Verena Schrameyer, Ove Hoeghguldberg
    Abstract:

    The broad range in physiological variation displayed by Symbiodinium spp. has proven imperative during periods of environmental change and contribute to the survival of their coral host. Characterizing how host and Symbiodinium community assemblages differ across environmentally distinct habitats provides useful information to predict how corals will respond to major environmental change. Despite the extensive characterizations of Symbiodinium diversity found amongst reef cnidarians on the Great Barrier Reef (GBR) substantial biogeographic gaps exist, especially across inshore habitats. Here, we investigate Symbiodinium community patterns in invertebrates from inshore and mid-shelf reefs on the southern GBR, Australia. Dominant Symbiodinium types were characterized using denaturing gradient gel electrophoresis fingerprinting and sequencing of the ITS2 region of the ribosomal DNA. Twenty one genetically distinct Symbiodinium types including four novel types were identified from 321 reef-invertebrate samples comprising three sub-generic clades (A, C, and D). A range of host genera harbored C22a, which is normally rare or absent from inshore or low latitude reefs in the GBR. Multivariate analysis showed that host identity and sea surface temperature best explained the variation in symbiont communities across sites. Patterns of changes in Symbiodinium community assemblage over small geographic distances (100s of kilometers or less) indicate the likelihood that shifts in Symbiodinium distributions and associated host populations, may occur in response to future climate change impacting the GBR.

  • transcriptomic characterization of the enzymatic antioxidants fesod mnsod apx and katg in the dinoflagellate genus Symbiodinium
    BMC Evolutionary Biology, 2015
    Co-Authors: William Leggat, Sophie Dove, Paul Fisher, Ove Hoeghguldberg, Thomas Krueger, Susanne Becker, Stefanie Pontasch, Simon K. Davy
    Abstract:

    The diversity of the symbiotic dinoflagellate Symbiodinium sp., as assessed by genetic markers, is well established. To what extent this diversity is reflected on the amino acid level of functional genes such as enzymatic antioxidants that play an important role in thermal stress tolerance of the coral-Symbiodinium symbiosis is, however, unknown. Here we present a predicted structural analysis and phylogenetic characterization of the enzymatic antioxidant repertoire of the genus Symbiodinium. We also report gene expression and enzymatic activity under short-term thermal stress in Symbiodinium of the B1 genotype. Based on eight different ITS2 types, covering six clades, multiple protein isoforms for three of the four investigated antioxidants (ascorbate peroxidase [APX], catalase peroxidase [KatG], manganese superoxide dismutase [MnSOD]) are present in the genus Symbiodinium. Amino acid sequences of both SOD metalloforms (Fe/Mn), as well as KatG, exhibited a number of prokaryotic characteristics that were also supported by the protein phylogeny. In contrast to the bacterial form, KatG in Symbiodinium is characterized by extended functionally important loops and a shortened C-terminal domain. Intercladal sequence variations were found to be much higher in both peroxidases, compared to SODs. For APX, these variable residues involve binding sites for substrates and cofactors, and might therefore differentially affect the catalytic properties of this enzyme between clades. While expression of antioxidant genes was successfully measured in Symbiodinium B1, it was not possible to assess the link between gene expression and protein activity due to high variability in expression between replicates, and little response in their enzymatic activity over the three-day experimental period. The genus Symbiodinium has a diverse enzymatic antioxidant repertoire that has similarities to prokaryotes, potentially as a result of horizontal gene transfer or events of secondary endosymbiosis. Different degrees of sequence evolution between SODs and peroxidases might be the result of potential selective pressure on the conserved molecular function of SODs as the first line of defence. In contrast, genetic redundancy of hydrogen peroxide scavenging enzymes might permit the observed variations in peroxidase sequences. Our data and successful measurement of antioxidant gene expression in Symbiodinium will serve as basis for further studies of coral health.

  • antioxidant plasticity and thermal sensitivity in four types of Symbiodinium sp
    Journal of Phycology, 2014
    Co-Authors: William Leggat, Sophie Dove, Paul Fisher, Ove Hoeghguldberg, Thomas Krueger, Susanne Becker, Stefanie Pontasch, Simon K. Davy
    Abstract:

    Warmer than average summer sea surface temperature is one of the main drivers for coraltemperature is one of the main drivers for coral bleaching, which describes the loss of endosymbiotic dinoflagellates (genus: Symbiodinium) in reef-building corals. Past research has established that oxidative stress in the symbiont plays an important part in the bleaching cascade. Corals hosting different genotypes of Symbiodinium may have varying thermal bleaching thresholds, but changes in the symbiont's antioxidant system that may accompany these differences have received less attention. This study shows that constitutive activity and up-regulation of different parts of the antioxidant network under thermal stress differs between four Symbiodinium types in culture and that thermal susceptibility can be linked to glutathione redox homeostasis. In Symbiodinium B1, C1 and E, declining maximum quantum yield of PSII (F-v/F-m) and death at 33 degrees C were generally associated with elevated superoxide dismutase (SOD) activity and a more oxidized glutathione pool. Symbiodinium F1 exhibited no decline in F-v/F-m or growth, but showed proportionally larger increases in ascorbate peroxidase (APX) activity and glutathione content (GSx), while maintaining GSx in a reduced state. Depressed growth in Symbiodinium B1 at a sublethal temperature of 29 degrees C was associated with transiently increased APX activity and glutathione pool size, and an overall increase in glutathione reductase (GR) activity. The collapse of GR activity at 33 degrees C, together with increased SOD, APX and glutathione S-transferase activity, contributed to a strong oxidation of the glutathione pool with subsequent death. Integrating responses of multiple components of the antioxidant network highlights the importance of antioxidant plasticity in explaining type-specific temperature responses in Symbiodinium.

  • Symbiodinium dinophyceae diversity in reef invertebrates along an offshore to inshore reef gradient near lizard island great barrier reef
    Journal of Phycology, 2014
    Co-Authors: Linda Tonk, Eugenia M Sampayo, Verena Schrameyer, Todd C Lajeunesse, Ove Hoeghguldberg
    Abstract:

    Despite extensive work on the genetic diversity of reef invertebrate-dinoflagellate symbioses on the Great Barrier Reef (GBR; Australia), large information gaps exist from northern and inshore regions. Therefore, a broad survey was done comparing the community of inshore, mid-shelf and outer reefs at the latitude of Lizard Island. Symbiodinium (Freudenthal) diversity was characterized using denaturing gradient gel electrophoresis fingerprinting and sequencing of the ITS2 region of the ribosomal DNA. Thirty-nine distinct Symbiodinium types were identified from four subgeneric clades (B, C, D, and G). Several Symbiodinium types originally characterized from the Indian Ocean were discovered as well as eight novel types (C1kk, C1LL, C3nn, C26b, C161a, C162, C165, C166). Multivariate analyses on the Symbiodinium species diversity data showed a strong link with host identity, consistent with previous findings. Of the four environmental variables tested, mean austral winter sea surface temperature (SST) influenced Symbiodinium distribution across shelves most significantly. A similar result was found when the analysis was performed on Symbiodinium diversity data of genera with an open symbiont transmission mode separately with chl a and PAR explaining additional variation. This study underscores the importance of SST and water quality related variables as factors driving Symbiodinium distribution on cross-shelf scales. Furthermore, this study expands our knowledge on Symbiodinium species diversity, ecological partitioning (including host-specificity) and geographic ranges across the GBR. The accelerating rate of environmental change experienced by coral reef ecosystems emphasizes the need to comprehend the full complexity of cnidarian symbioses, including the biotic and abiotic factors that shape their current distributions.

  • sharing the slope depth partitioning of agariciid corals and associated Symbiodinium across shallow and mesophotic habitats 2 60 m on a caribbean reef
    BMC Evolutionary Biology, 2013
    Co-Authors: Pim Bongaerts, Pedro R Frade, Julie J Ogier, Kyra B Hay, Judith Van Bleijswijk, Norbert Englebert, Mark J A Vermeij, Rolf P M Bak, Petra M Visser, Ove Hoeghguldberg
    Abstract:

    Background: Scleractinian corals and their algal endosymbionts (genus Symbiodinium) exhibit distinct bathymetric distributions on coral reefs. Yet, few studies have assessed the evolutionary context of these ecological distributions by exploring the genetic diversity of closely related coral species and their associated Symbiodinium over large depth ranges. Here we assess the distribution and genetic diversity of five agariciid coral species (Agaricia humilis, A. agaricites, A. lamarcki, A. grahamae, and Helioseris cucullata) and their algal endosymbionts (Symbiodinium) across a large depth gradient (2-60 m) covering shallow to mesophotic depths on a Caribbean reef. Results: The five agariciid species exhibited distinct depth distributions, and dominant Symbiodinium associations were found to be species-specific, with each of the agariciid species harbouring a distinct ITS2-DGGE profile (except for a shared profile between A. lamarcki and A. grahamae). Only A. lamarcki harboured different Symbiodinium types across its depth distribution (i.e. exhibited symbiont zonation). Phylogenetic analysis (atp6) of the coral hosts demonstrated a division of the Agaricia genus into two major lineages that correspond to their bathymetric distribution (“shallow”: A. humilis / A. agaricites and “deep”: A. lamarcki / A. grahamae), highlighting the role of depth-related factors in the diversification of these congeneric agariciid species. The divergence between “shallow” and “deep” host species was reflected in the relatedness of the associated Symbiodinium (with A. lamarcki and A. grahamae sharing an identical Symbiodinium profile, and A. humilis and A. agaricites harbouring a related ITS2 sequence in their Symbiodinium profiles), corroborating the notion that brooding corals and their Symbiodinium are engaged in coevolutionary processes. Conclusions: Our findings support the hypothesis that the depth-related environmental gradient on reefs has played an important role in the diversification of the genus Agaricia and their associated Symbiodinium, resulting in a genetic segregation between coral host-symbiont communities at shallow and mesophotic depths.

Mary Alice Coffroth - One of the best experts on this subject based on the ideXlab platform.

  • taxonomic and environmental variation of metabolite profiles in marine dinoflagellates of the genus Symbiodinium
    Metabolites, 2015
    Co-Authors: Anke Klueter, Jesse Ben Crandall, Frederick I Archer, Mark A Teece, Mary Alice Coffroth
    Abstract:

    Microorganisms in terrestrial and marine ecosystems are essential to environmental sustainability. In the marine environment, invertebrates often depend on metabolic cooperation with their endosymbionts. Coral reefs, one of the most important marine ecosystems, are based on the symbiosis between a broad diversity of dinoflagellates of the genus Symbiodinium and a wide phyletic diversity of hosts (i.e., cnidarian, molluscan, poriferan). This diversity is reflected in the ecology and physiology of the symbionts, yet the underlying biochemical mechanisms are still poorly understood. We examined metabolite profiles of four cultured species of Symbiodinium known to form viable symbioses with reef-building corals, S. microadriaticum (cp-type A194), S. minutum (cp-type B184), S. psygmophilum (cp-type B224) and S. trenchii (cp-type D206). Metabolite profiles were shown to differ among Symbiodinium species and were found to be affected by their physiological response to growth in different temperatures and light regimes. A combined Random Forests and Bayesian analysis revealed that the four Symbiodinium species examined primarily differed in their production of sterols and sugars, including a C29 stanol and the two sterols C28Δ5 and C28Δ5,22, as well as differences in metabolite abundances of a hexose and inositol. Inositol levels were also strongly affected by changes in temperature across all Symbiodinium species. Our results offer a detailed view of the metabolite profile characteristic of marine symbiotic dinoflagellates of the genus Symbiodinium, and identify patterns of metabolites related to several growth conditions.

  • Symbiodinium transcriptomes genome insights into the dinoflagellate symbionts of reef building corals
    PLOS ONE, 2012
    Co-Authors: Till Bayer, Christian R. Voolstra, Manuel Aranda, Mary Alice Coffroth, Michael K Desalvo, Shinichi Sunagawa, Erika Lindquist, Monica Medina
    Abstract:

    Dinoflagellates are unicellular algae that are ubiquitously abundant in aquatic environments. Species of the genus Symbiodinium form symbiotic relationships with reef-building corals and other marine invertebrates. Despite their ecologic importance, little is known about the genetics of dinoflagellates in general and Symbiodinium in particular. Here, we used 454 sequencing to generate transcriptome data from two Symbiodinium species from different clades (clade A and clade B). With more than 56,000 assembled sequences per species, these data represent the largest transcriptomic resource for dinoflagellates to date. Our results corroborate previous observations that dinoflagellates possess the complete nucleosome machinery. We found a complete set of core histones as well as several H3 variants and H2A.Z in one species. Furthermore, transcriptome analysis points toward a low number of transcription factors in Symbiodinium spp. that also differ in the distribution of DNA-binding domains relative to other eukaryotes. In particular the cold shock domain was predominant among transcription factors. Additionally, we found a high number of antioxidative genes in comparison to non-symbiotic but evolutionary related organisms. These findings might be of relevance in the context of the role that Symbiodinium spp. play as coral symbionts. Our data represent the most comprehensive dinoflagellate EST data set to date. This study provides a comprehensive resource to further analyze the genetic makeup, metabolic capacities, and gene repertoire of Symbiodinium and dinoflagellates. Overall, our findings indicate that Symbiodinium possesses some unique characteristics, in particular the transcriptional regulation in Symbiodinium may differ from the currently known mechanisms of eukaryotic gene regulation.

  • isolation and characterization of microsatellite loci in Symbiodinium b1 b184 the dinoflagellate symbiont of the caribbean sea fan coral gorgonia ventalina
    Molecular Ecology Resources, 2009
    Co-Authors: Jason P. Andras, Mary Alice Coffroth, Nathan L. Kirk, Drew C Harvell
    Abstract:

    Here we report primers targeting 10 microsatellite loci of dinoflagellates in the genus Symbiodinium (clade B1/B184) symbiotic with the Caribbean sea fan coral, Gorgonia ventalina. Primers were tested on 12 Symbiodinium B1/B184 cultures, as well as 40 genomic DNA extracts of G. ventalina tissue samples. All loci were polymorphic with allelic richness ranging from 4-16. Gene diversity ranged from 0.15 to 0.91. These primers provide powerful tools for examining the fine-scale population structure and dynamics of Symbiodinium within a single host species.

  • population structure of Symbiodinium sp associated with the common sea fan gorgonia ventalina in the florida keys across distance depth and time
    Marine Biology, 2009
    Co-Authors: Scott R Santos, Jason P. Andras, Nathan L. Kirk, Drew C Harvell, Mary Alice Coffroth
    Abstract:

    Numerous marine invertebrates form endosymbiotic relationships with dinoflagellates in the genus Symbiodinium. However, few studies have examined the fine-scale population structure of these symbionts. Here, we describe the genetic structure of Symbiodinium type “B1/B184” inhabiting the gorgonian Gorgoniaventalina along the Florida Keys. Six polymorphic microsatellite loci were utilized to examine 16 populations along the Upper, Middle, and Lower Keys spanning a range of ~200 km. Multiple statistical tests detected significant differentiation in 54–92% of the 120 possible pairwise comparisons between localities, suggesting low levels of gene flow in these dinoflagellates. In general, populations clustered by geographic region and/or reefs in close proximity. Some of the sharpest population differentiation was detected between Symbiodinium from deep and shallow sites on the same reef. In spite of the high degree of population structure, alleles and genotypes were shared among localities, indicating some connectivity between Symbiodinium populations associated with G. ventalina.

  • fine scale diversity and specificity in the most prevalent lineage of symbiotic dinoflagellates Symbiodinium dinophyceae of the caribbean
    Molecular Ecology, 2004
    Co-Authors: Scott R Santos, T L Shearer, A R Hannes, Mary Alice Coffroth
    Abstract:

    The success of coral reefs is due to obligate mutualistic symbioses involving invertebrates and photosynthetic dinoflagellate symbionts belonging to the genus Symbiodinium . In the Caribbean, the vast majority of octocorals and other invertebrate hosts associate with Symbiodinium clade B, and more selectively, with a single lineage of this clade, Symbiodinium B1/B184. Although B1/B184 represents the most prevalent Symbiodinium in the Caribbean, there is little evidence supporting fine-scale diversity and host–alga specificity within this lineage. We explored simultaneously the questions of diversity and specificity in Symbiodinium B1/B184 by sequencing the flanking regions of two polymorphic microsatellites from a series of Symbiodinium clade B cultures along with Symbiodinium B1/B184 populations of the octocorals Pseudopterogorgia elisabethae , P. bipinnata and Gorgonia ventalina . Seven unique sequence variants were identified based on concatenation of the two loci. Phylogenetic analyses of these variants, which we refer to as phylotypes, recognized five as belonging to B1/B184, thus providing the first evidence of distinct taxa within this Symbiodinium lineage. Furthermore, sympatric P. elisabethae and P. bipinnata at San Salvador in the Bahamas were found to harbour distinct Symbiodinium B1/B184 phylotypes, demonstrating unequivocally the existence of fine-scale specificity between Caribbean octocorals and these algae. Taken together, this study exemplifies the complex nature of Symbiodinium biodiversity and specificity.

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  • unexpected mixed mode transmission and moderate genetic regulation of Symbiodinium communities in a brooding coral
    bioRxiv, 2017
    Co-Authors: Patricia A Warner, Kate M Quigley, Bette L Willis
    Abstract:

    Determining the extent to which Symbiodinium communities in corals are inherited versus environmentally-acquired is fundamental to understanding coral resilience and to predicting coral responses to stressors like warming oceans that disrupt this critical endosymbiosis. We examined the fidelity with which Symbiodinium communities in the brooding coral Seriatopora hystrix are vertically transmitted and the extent to which communities are genetically regulated, by genotyping 60 larvae and their parents (9 maternal and 45 paternal colonies) using high throughput sequencing of the ITS-2 locus. Unexpectedly, Symbiodinium communities associated with brooded larvae were distinct from those within parent colonies, including the presence of types not detected in adults. Bayesian heritability (h2) analysis revealed that 33% of variability in larval Symbiodinium communities was genetically controlled. Results highlight flexibility in the establishment of larval communities and overturn the paradigm that symbiont transmission is exclusively vertical in brooding corals. Instead, we show that Symbiodinium transmission in S. hystrix involves a mixed-mode strategy, similar to many terrestrial invertebrate symbioses. Also, variation in the abundances of common Symbiodinium types among adult communities suggests that microhabitat differences influence the structure of in hospite Symbiodinium communities. Partial genetic regulation coupled with flexibility in the environmentally-acquired component of larval Symbiodinium communities implies that corals with vertical transmission, like S. hystrix, may be more resilient to environmental change than previously thought.

  • heritability of the Symbiodinium community in vertically and horizontally transmitting broadcast spawning corals
    bioRxiv, 2017
    Co-Authors: Kate M Quigley, Bette L Willis, Line K Bay
    Abstract:

    The dinoflagellate-coral partnership influences host tolerance to thermal stress that causes bleaching. However, the comparative roles of host genetic versus environmental factors in determining the composition of this symbiosis are largely unknown. Here we quantify the heritability of Symbiodinium communities in two broadcast spawning corals with different symbiont transmission modes: Acropora tenuis has environmental acquisition, and Montipora digitata has maternal transmission. Using high throughput sequencing of the ITS-2 region to characterize communities in parental colonies, juveniles and eggs, we describe new Symbiodinium types in both coral species and previously unknown symbiont dynamics. After one month of natural uptake in the field, Symbiodinium communities associated with A. tenuis juveniles were dominated by A3, C1, D1, A-type CCMP828, and D1a in proportional abundances that were conserved across two years. In contrast, M. digitata eggs were characterized by C15, D1, and A3. On average, host genetic influences accounted for 29% of phenotypic variation found in Symbiodinium communities in A. tenuis and 62% in M. digitata . Our results reveal hitherto unknown flexibility in the acquisition of Symbiodinium communities and substantial heritability in both species provides ample material for selection to produce partnerships that are locally adapted to changing environmental conditions.

  • deep sequencing method for quantifying background abundances of Symbiodinium types exploring the rare Symbiodinium biosphere in reef building corals
    PLOS ONE, 2014
    Co-Authors: Kate M Quigley, Bette L Willis, Sarah W Davies, Carly D Kenkel, Mikhail V Matz, Line K Bay
    Abstract:

    The capacity of reef-building corals to associate with environmentally-appropriate types of endosymbionts from the dinoflagellate genus Symbiodinium contributes significantly to their success at local scales. Additionally, some corals are able to acclimatize to environmental perturbations by shuffling the relative proportions of different Symbiodinium types hosted. Understanding the dynamics of these symbioses requires a sensitive and quantitative method of Symbiodinium genotyping. Electrophoresis methods, still widely utilized for this purpose, are predominantly qualitative and cannot guarantee detection of a background type below 10% of the total Symbiodinium population. Here, the relative abundances of four Symbiodinium types (A13, C1, C3, and D1) in mixed samples of known composition were quantified using deep sequencing of the internal transcribed spacer of the ribosomal RNA gene (ITS-2) by means of Next Generation Sequencing (NGS) using Roche 454. In samples dominated by each of the four Symbiodinium types tested, background levels of the other three types were detected when present at 5%, 1%, and 0.1% levels, and their relative abundances were quantified with high (A13, C1, D1) to variable (C3) accuracy. The potential of this deep sequencing method for resolving fine-scale genetic diversity within a symbiont type was further demonstrated in a natural symbiosis using ITS-1, and uncovered reef-specific differences in the composition of Symbiodinium microadriaticum in two species of acroporid corals (Acropora digitifera and A. hyacinthus) from Palau. The ability of deep sequencing of the ITS locus (1 and 2) to detect and quantify low-abundant Symbiodinium types, as well as finer-scale diversity below the type level, will enable more robust quantification of local genetic diversity in Symbiodinium populations. This method will help to elucidate the role that background types have in maximizing coral fitness across diverse environments and in response to environmental change.

  • infection dynamics vary between Symbiodinium types and cell surface treatments during establishment of endosymbiosis with coral larvae
    Diversity, 2011
    Co-Authors: Bette L Willis, Line K Bay, David Abrego, Vivian R Cumbo, Johnathan Kool, Tracy D Ainsworth
    Abstract:

    Symbioses between microbes and higher organisms underpin high diversity in many ecosystems, including coral reefs, however mechanisms underlying the early establishment of symbioses remain unclear. Here we examine the roles of Symbiodinium type and cell surface recognition in the establishment of algal endosymbiosis in the reef-building coral, Acropora tenuis. We found 20–70% higher infection success (proportion of larvae infected) and five-fold higher Symbiodinium abundance in larvae exposed to ITS-1 type C1 compared to ITS-1 type D in the first 96 h following exposure. The highest abundance of Symbiodinium within larvae occurred when C1-type cells were treated with enzymes that modified the 40–100 kD glycome, including glycoproteins and long chain starch residues. Our finding of declining densities of Symbiodinium C1 through time in the presence of intact cell surface molecules supports a role for cell surface recognition molecules in controlling post-phagocytosis processes, leading to rejection of some Symbiodinium types in early ontogeny. Reductions in the densities of unmodified C1 symbionts after 96 h, in contrast to increases in D symbionts may suggest the early initiation of a winnowing process contributing to the establishment of Symbiodinium D as the dominant type in one-month old juveniles of A. tenuis.

  • onset of algal endosymbiont specificity varies among closely related species of acropora corals during early ontogeny
    Molecular Ecology, 2009
    Co-Authors: David Abrego, Bette L Willis, Madeleine J. H. Van Oppen
    Abstract:

    Juveniles of a number of corals with horizontal transmission of dinoflagellate endosymbionts naturally acquire and maintain Symbiodinium types that differ from those found in adult populations. However, the duration of this early period of symbiont flexibility and successional changes leading to dominance by the characteristic adult (homologous) type are unknown. To document natural succession of Symbiodinium types within juvenile corals, we monitored Symbiodinium communities in juveniles of Acropora tenuis and Acropora millepora for 3.5 years. Juveniles originating from one of three reef populations, characterized by differing adult coral-Symbiodinium associations, were raised in a common environment. In four out of five cases, juveniles became dominated initially by a nonhomologous adult type. Changes in Symbiodinium communities associated with A. tenuis juveniles led to the establishment of the adult homologous association at approximately 3.5 years of age. These changes were not linked to the onset of reproductive maturity, but may be linked to micro-environmental changes associated with vertical growth of juvenile corals. We hypothesize that fine-tuning of specificity mechanisms takes place during ontogeny in A. tenuis, leading to the eventual establishment of the adult homologous association. However, Symbiodinium communities in A. millepora juveniles did not change significantly over the 3.5 years, potentially reflecting (i) lack of specificity, (ii) more than a 3.5-year delay in the onset of specificity, or (iii) lack of availability of the adult Symbiodinium type. This study demonstrates that juvenile corals may survive for extended periods of time with nonhomologous Symbiodinium types and that closely related species of Acropora differ in the timing of the onset of specificity for algal symbionts.