Publications by authors named "Mary Alice Coffroth"

30 Publications

  • Page 1 of 1

Competition and succession among coral endosymbionts.

Ecol Evol 2019 Nov 30;9(22):12767-12778. Epub 2019 Oct 30.

Graduate Program in Evolution, Ecology and Behavior State University of New York University at Buffalo Buffalo New York.

Host species often support a genetically diverse guild of symbionts, the identity and performance of which can determine holobiont fitness under particular environmental conditions. These symbiont communities are structured by a complex set of potential interactions, both positive and negative, between the host and symbionts and among symbionts. In reef-building corals, stable associations with specific symbiont species are common, and we hypothesize that this is partly due to ecological mechanisms, such as succession and competition, which drive patterns of symbiont winnowing in the initial colonization of new generations of coral recruits. We tested this hypothesis using the experimental framework of the de Wit replacement series and found that competitive interactions occurred among symbionts which were characterized by unique ecological strategies. Aposymbiotic octocoral recruits within high- and low-light environments were inoculated with one of three Symbiodiniaceae species as monocultures or with cross-paired mixtures, and we tracked symbiont uptake using quantitative genetic assays. Priority effects, in which early colonizers excluded competitive dominants, were evidenced under low light, but these early opportunistic species were later succeeded by competitive dominants. Under high light, a more consistent competitive hierarchy was established in which competitive dominants outgrew and limited the abundance of others. These findings provide insight into mechanisms of microbial community organization and symbiosis breakdown and recovery. Furthermore, transitions in competitive outcomes across spatial and temporal environmental variation may improve lifetime host fitness.
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http://dx.doi.org/10.1002/ece3.5749DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6875658PMC
November 2019

Genetic variation in , a coral reef symbiont, in response to temperature and nutrients.

Ecol Evol 2019 Mar 7;9(5):2803-2813. Epub 2019 Feb 7.

Biology Department California State University Northridge California.

Symbionts within the family are important on coral reefs because they provide significant amounts of carbon to many different reef species. The breakdown of this mutualism that occurs as a result of increasingly warmer ocean temperatures is a major threat to coral reef ecosystems globally. Recombination during sexual reproduction and high rates of somatic mutation can lead to increased genetic variation within symbiont species, which may provide the fuel for natural selection and adaptation. However, few studies have asked whether such variation in functional traits exists within these symbionts. We used several genotypes of two closely related species, and , to examine variation of traits related to symbiosis in response to increases in temperature or nitrogen availability in laboratory cultures. We found significant genetic variation within and among symbiont species in chlorophyll content, photosynthetic efficiency, and growth rate. Two genotypes showed decreases in traits in response to increased temperatures predicted by climate change, but one genotype responded positively. Similarly, some genotypes within a species responded positively to high-nitrogen environments, such as those expected within hosts or eutrophication associated with global change, while other genotypes in the same species responded negatively, suggesting context-dependency in the strength of mutualism. Such variation in traits implies that there is potential for natural selection on symbionts in response to temperature and nutrients, which could confer an adaptive advantage to the holobiont.
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http://dx.doi.org/10.1002/ece3.4959DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6406013PMC
March 2019

Revisiting "Genetic Diversity of Symbiotic Dinoflagellates in the Genus Symbiodinium".

Protist 2018 11 6;169(5):784-787. Epub 2018 Jul 6.

Department of Geology, Graduate Program in Evolution, Ecology and Behavior, State University of New York at Buffalo, Buffalo, NY 14260, USA.

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http://dx.doi.org/10.1016/j.protis.2018.06.008DOI Listing
November 2018

Comparative growth rates of cultured marine dinoflagellates in the genus Symbiodinium and the effects of temperature and light.

PLoS One 2017 29;12(11):e0187707. Epub 2017 Nov 29.

Graduate Program in Evolution, Ecology and Behavior, State University of New York at Buffalo, Buffalo, New York, United States of America.

Many dinoflagellate microalgae of the genus Symbiodinium form successful symbioses with a large group of metazoans and selected protists. Yet knowledge of growth kinetics of these endosymbionts and their ecological and evolutionary implications is limited. We used a Bayesian biphasic generalized logistic model to estimate key parameters of the growth of five strains of cultured Symbiodinium, S. microadriaticum (cp-type A194; strain 04-503), S. microadriaticum (cp-type A194; strain CassKB8), S. minutum (cp-type B184; strain Mf 1.05b.01.SCI.01), S. psygmophilum (cp-type B224; strain Mf 11.05b.01) and S. trenchii (cp-type D206; strain Mf 2.2b), grown in four different combinations of temperature and light. Growth kinetics varied among Symbiodinium strains and across treatments. Biphasic growth was especially evident for S. minutum and S. psygmophilum across all treatments. Monophasic growth was more common when final asymptotic densities were relatively low (~ 200 million cells ml-1). All species tended to grow faster and / or reached a higher asymptote at 26°C than at 18°C. The fastest growth was exhibited by S. minutum, with an approximate four-fold increase in estimated cell density after 60 days. The strongest effect of light was seen in S. trenchii, in which increasing light levels resulted in a decrease in initial growth rate, and an increase in asymptotic density, time when growth rate was at its maximum, final growth rate, and maximum growth rate. Results suggest that Symbiodinium species have different photokinetic and thermal optima, which may affect their growth-related nutritional physiology and allow them to modify their response to environmental changes.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0187707PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5706665PMC
December 2017

Caribbean massive corals not recovering from repeated thermal stress events during 2005-2013.

Ecol Evol 2017 03 1;7(5):1339-1353. Epub 2017 Feb 1.

The Scripps Institution for Oceanography University of California San Diego La Jolla CA USA; Smithsonian Tropical Research Institute Ancon Republic of Panama.

Massive coral bleaching events associated with high sea surface temperatures are forecast to become more frequent and severe in the future due to climate change. Monitoring colony recovery from bleaching disturbances over multiyear time frames is important for improving predictions of future coral community changes. However, there are currently few multiyear studies describing long-term outcomes for coral colonies following acute bleaching events. We recorded colony pigmentation and size for bleached and unbleached groups of co-located conspecifics of three major reef-building scleractinian corals (, ;  = 198 total) in Bocas del Toro, Panama, during the major 2005 bleaching event and then monitored pigmentation status and changes live tissue colony size for 8 years (2005-2013). Corals that were bleached in 2005 demonstrated markedly different response trajectories compared to unbleached colony groups, with extensive live tissue loss for bleached corals of all species following bleaching, with mean live tissue losses per colony 9 months postbleaching of 26.2% (±5.4 ) for 35.7% (±4.7 ) for , and 11.2% (±3.9 ) for . Two species, and , later recovered to net positive growth, which continued until a second thermal stress event in 2010. Following this event, all species again lost tissue, with previously unbleached colony species groups experiencing greater declines than conspecific sample groups, which were previously bleached, indicating a possible positive acclimative response. However, despite this beneficial effect for previously bleached corals, all groups experienced substantial net tissue loss between 2005 and 2013, indicating that many important Caribbean reef-building corals will likely suffer continued tissue loss and may be unable to maintain current benthic coverage when faced with future thermal stress forecast for the region, even with potential benefits from bleaching-related acclimation.
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http://dx.doi.org/10.1002/ece3.2706DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5330915PMC
March 2017

The effects of Symbiodinium (Pyrrhophyta) identity on growth, survivorship, and thermal tolerance of newly settled coral recruits.

J Phycol 2016 12 8;52(6):1114-1124. Epub 2016 Nov 8.

Graduate Program in Evolution, Ecology, and Behavior, University at Buffalo, 126 Cooke Hall, Buffalo, New York, 14260, USA.

For many coral species, the obligate association with phylogenetically diverse algal endosymbiont species is dynamic in time and space. Here, we used controlled laboratory inoculations of newly settled, aposymbiotic corals (Orbicella faveolata) with two cultured species of algal symbiont (Symbiodinium microadriaticum and S. minutum) to examine the role of symbiont identity on growth, survivorship, and thermal tolerance of the coral holobiont. We evaluated these data in the context of Symbiodinium photophysiology for 9 months post-settlement and also during a 5-d period of elevated temperatures Our data show that recruits that were inoculated with S. minutum grew significantly slower than those inoculated with S. microadriaticum (occasionally co-occurring with S. minutum), but that there was no difference in survivorship of O. faveolata polyps infected with Symbiodinium. However, photophysiological metrics (∆Fv/F'm, the efficiency with which available light is used to drive photosynthesis and α, the maximum light utilization coefficient) were higher in those slower growing recruits containing S. minutum. These findings suggest that light use (i.e., photophysiology) and carbon acquisition by the coral host (i.e., host growth) are decoupled, but did not distinguish the source of this difference. Neither Symbiodinium treatment demonstrated a significant negative effect of a 5-d exposure to temperatures as high as 32°C under low light conditions similar to those measured at settlement habitats.
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http://dx.doi.org/10.1111/jpy.12471DOI Listing
December 2016

New species of Clade B Symbiodinium (Dinophyceae) from the greater Caribbean belong to different functional guilds: S. aenigmaticum sp. nov., S. antillogorgium sp. nov., S. endomadracis sp. nov., and S. pseudominutum sp. nov.

J Phycol 2015 Oct 13;51(5):850-8. Epub 2015 Sep 13.

Department of Biology, The Pennsylvania State University, University Park, Pennsylvania, 16802, USA.

Molecular approaches have begun to supersede traditional morphometrics in the species delineation of micro-eukaryotes. In addition to fixed differences in DNA sequences, recent genetics-based descriptions within the dinoflagellate genus Symbiodinium have incorporated confirmatory morphological, physiological, and ecological evidence when possible. However, morphological and physiological data are difficult to collect from species that have not been cultured, while the natural ecologies of many cultured species remain unknown. Here, we rely on genetic evidence-the only data consistently available among all taxa investigated-to describe four new Clade B Symbiodinium species. The 'host-specialized' species (S. antillogorgium sp. nov. and S. endomadracis sp. nov.) engage in mutualisms with specific cnidarian hosts, but exhibit differences in our ability to culture them in vitro. The ecologically 'cryptic' species (S. aenigmaticum sp. nov. and S. pseudominutum sp. nov.) thrive in culture, but their roles or functions in the ecosystem (i.e., niches) are yet to be documented. These new species call further attention to the spectrum of ecological guilds among Symbiodinium.
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http://dx.doi.org/10.1111/jpy.12340DOI Listing
October 2015

Taxonomic and environmental variation of metabolite profiles in marine dinoflagellates of the genus symbiodinium.

Metabolites 2015 Feb 16;5(1):74-99. Epub 2015 Feb 16.

SUNY-University at Buffalo, Graduate Program in Evolution, Ecology and Behavior and Department of Geology, Buffalo, NY 14260, USA.

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.
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http://dx.doi.org/10.3390/metabo5010074DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4381291PMC
February 2015

Cryptic diversity hides host and habitat specialization in a gorgonian-algal symbiosis.

Mol Ecol 2014 07 16;23(13):3330-40. Epub 2014 Jun 16.

Department of Biological Sciences, Louisiana State University, Baton Rouge, LA, 70803, USA.

Shallow water anthozoans, the major builders of modern coral reefs, enhance their metabolic and calcification rates with algal symbionts. Controversy exists over whether these anthozoan-algae associations are flexible over the lifetimes of individual hosts, promoting acclimative plasticity, or are closely linked, such that hosts and symbionts co-evolve across generations. Given the diversity of algal symbionts and the morphological plasticity of many host species, cryptic variation within either partner could potentially confound studies of anthozoan-algal associations. Here, we used ribosomal, organelle and nuclear sequences, along with microsatellite variation, to study the relationship between lineages of a common Caribbean gorgonian and its algal symbionts. The gorgonian Eunicea flexuosa is a broadcast spawner, composed of two recently diverged, genetically distinct lineages largely segregated by depth. We sampled colonies of the two lineages across depth gradients at three Caribbean locations. We find that each host lineage is associated with a unique Symbiodinium B1/184 phylotype. This relationship between host and symbiont is maintained when host colonies are reciprocally transplanted, although cases of within phylotype switching were also observed. Even when the phylotypes of both partners are present at intermediate depths, the specificity between host and symbiont lineages remained absolute. Unrecognized cryptic diversity may mask host-symbiont specificity and change the inference of evolutionary processes in mutualistic associations. Symbiotic specificity thus likely contributes to the ecological divergence of the two partners, generating species diversity within coral reefs.
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http://dx.doi.org/10.1111/mec.12808DOI Listing
July 2014

Tracking transmission of apicomplexan symbionts in diverse Caribbean corals.

PLoS One 2013 19;8(11):e80618. Epub 2013 Nov 19.

Auburn University, Department of Biological Sciences and Molette Biology Laboratory for Environmental and Climate Change Studies, Auburn, Alabama, United States of America.

Symbionts in each generation are transmitted to new host individuals either vertically (parent to offspring), horizontally (from exogenous sources), or a combination of both. Scleractinian corals make an excellent study system for understanding patterns of symbiont transmission since they harbor diverse symbionts and possess distinct reproductive modes of either internal brooding or external broadcast spawning that generally correlate with vertical or horizontal transmission, respectively. Here, we focused on the under-recognized, but apparently widespread, coral-associated apicomplexans (Protista: Alveolata) to determine if symbiont transmission depends on host reproductive mode. Specifically, a PCR-based assay was utilized towards identifying whether planula larvae and reproductive adults from brooding and broadcast spawning scleractinian coral species in Florida and Belize harbored apicomplexan DNA. Nearly all (85.5%; n = 85/89) examined planulae of five brooding species (Porites astreoides, Agaricia tenuifolia, Agaricia agaricites, Favia fragum, Mycetophyllia ferox) and adults of P. astreoides were positive for apicomplexan DNA. In contrast, no (n = 0/10) apicomplexan DNA was detected from planulae of four broadcast spawning species (Acropora cervicornis, Acropora palmata, Pseudodiploria strigosa, and Orbicella faveolata) and rarely in gametes (8.9%; n = 5/56) of these species sampled from the same geographical range as the brooding species. In contrast, tissue samples from nearly all (92.0%; n = 81/88) adults of the broadcast spawning species A. cervicornis, A. palmata and O. faveolata harbored apicomplexan DNA, including colonies whose gametes and planulae tested negative for these symbionts. Taken together, these data suggest apicomplexans are transmitted vertically in these brooding scleractinian coral species while the broadcast spawning scleractinian species examined here acquire these symbionts horizontally. Notably, these transmission patterns are consistent with those of other scleractinian coral symbionts. While this study furthers knowledge regarding these symbionts, numerous questions remain to be addressed, particularly in regard to the specific interaction(s) between these apicomplexans and their hosts.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0080618PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3833926PMC
August 2014

Draft assembly of the Symbiodinium minutum nuclear genome reveals dinoflagellate gene structure.

Curr Biol 2013 Aug 11;23(15):1399-408. Epub 2013 Jul 11.

Marine Genomics Unit, Okinawa Institute of Science and Technology Graduate University, Onna, Okinawa 904-0495, Japan.

Background: Dinoflagellates are known for their capacity to form harmful blooms (e.g., "red tides") and as symbiotic, photosynthetic partners for corals. These unicellular eukaryotes have permanently condensed, liquid-crystalline chromosomes and immense nuclear genome sizes, often several times the size of the human genome. Here we describe the first draft assembly of a dinoflagellate nuclear genome, providing insights into its genome organization and gene inventory.

Results: Sequencing reads from Symbiodinium minutum were assembled into 616 Mbp gene-rich DNA regions that represented roughly half of the estimated 1,500 Mbp genome of this species. The assembly encoded ∼42,000 protein-coding genes, consistent with previous dinoflagellate gene number estimates using transcriptomic data. The Symbiodinium genome contains duplicated genes for regulator of chromosome condensation proteins, nearly one-third of which have eukaryotic orthologs, whereas the remainder have most likely been acquired through bacterial horizontal gene transfers. Symbiodinium genes are enriched in spliceosomal introns (mean = 18.6 introns/gene). Donor and acceptor splice sites are unique, with 5' sites utilizing not only GT but also GC and GA, whereas at 3' sites, a conserved G is present after AG. All spliceosomal snRNA genes (U1-U6) are clustered in the genome. Surprisingly, the Symbiodinium genome displays unidirectionally aligned genes throughout the genome, forming a cluster-like gene arrangement.

Conclusions: We show here that a dinoflagellate genome exhibits unique and divergent characteristics when compared to those of other eukaryotes. Our data elucidate the organization and gene inventory of dinoflagellates and lay the foundation for future studies of this remarkable group of eukaryotes.
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http://dx.doi.org/10.1016/j.cub.2013.05.062DOI Listing
August 2013

Evaluating the ribosomal internal transcribed spacer (ITS) as a candidate dinoflagellate barcode marker.

PLoS One 2012 16;7(8):e42780. Epub 2012 Aug 16.

The Laboratory, Sir Alister Hardy Foundation for Ocean Science, Plymouth, United Kingdom.

Background: DNA barcoding offers an efficient way to determine species identification and to measure biodiversity. For dinoflagellates, an ancient alveolate group of about 2000 described extant species, DNA barcoding studies have revealed large amounts of unrecognized species diversity, most of which is not represented in culture collections. To date, two mitochondrial gene markers, Cytochrome Oxidase I (COI) and Cytochrome b oxidase (COB), have been used to assess DNA barcoding in dinoflagellates, and both failed to amplify all taxa and suffered from low resolution. Nevertheless, both genes yielded many examples of morphospecies showing cryptic speciation and morphologically distinct named species being genetically similar, highlighting the need for a common marker. For example, a large number of cultured Symbiodinium strains have neither taxonomic identification, nor a common measure of diversity that can be used to compare this genus to other dinoflagellates.

Methodology/principal Findings: The purpose of this study was to evaluate the Internal Transcribed Spacer units 1 and 2 (ITS) of the rDNA operon, as a high resolution marker for distinguishing species dinoflagellates in culture. In our study, from 78 different species, the ITS barcode clearly differentiated species from genera and could identify 96% of strains to a known species or sub-genus grouping. 8.3% showed evidence of being cryptic species. A quarter of strains identified had no previous species identification. The greatest levels of hidden biodiversity came from Scrippsiella and the Pfiesteriaceae family, whilst Heterocapsa strains showed a high level of mismatch to their given species name.

Conclusions/significance: The ITS marker was successful in confirming species, revealing hidden diversity in culture collections. This marker, however, may have limited use for environmental barcoding due to paralogues, the potential for unidentifiable chimaeras and priming across taxa. In these cases ITS would serve well in combination with other markers or for specific taxon studies.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0042780PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3420951PMC
May 2013

Symbiodinium transcriptomes: genome insights into the dinoflagellate symbionts of reef-building corals.

PLoS One 2012 18;7(4):e35269. Epub 2012 Apr 18.

Red Sea Research Center, King Abdullah University of Science and Technology, Thuwal, Saudi Arabia.

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.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0035269PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3329448PMC
November 2012

Development of microsatellite markers as a molecular tool for conservation studies of the Mediterranean reef builder coral Cladocora caespitosa (Anthozoa, Scleractinia).

J Hered 2011 Sep-Oct;102(5):622-6. Epub 2011 Jul 21.

Departmento de Biodiversidad y Biología Evolutiva, Museo Nacional de Ciencias Naturales, José Gutiérrez Abascal 2, Madrid, Spain.

Cladocora caespitosa is a reef-building zooxanthellate scleractinian coral in the Mediterranean Sea. Mortality events have recurrently affected this species during the last decade. Thus, knowledge of its genetic structure, population diversity, and connectivity is needed to accomplish suitable conservation plans. In order to obtain a better understanding of the population genetics of this species, 13 highly variable microsatellites markers were developed from a naturally bleached colony. The developed primers failed to amplify zooxanthella DNA, isolated from C. caespitosa, verifying that these markers were of the coral and not algal symbiont origin. The degree of polymorphism of these loci was tested on tissue samples from 28 colonies. The allele number for each loci ranged from 2 to 13 (mean N(a) = 5.4), with an average observed heterozygosity of 0.42 (H(e) = 0.43) and all loci were in Hardy-Weinberg equilibrium. These new markers should be useful in future conservation genetic studies and will help to improve the resolution of the individual identification within this coral species. Primers were also tested in Oculina patagonica, with successful amplifications of several loci.
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http://dx.doi.org/10.1093/jhered/esr070DOI Listing
December 2011

Rapid evolution of coral proteins responsible for interaction with the environment.

PLoS One 2011 25;6(5):e20392. Epub 2011 May 25.

Red Sea Research Center, King Abdullah University of Science and Technology, Thuwal, Saudi Arabia.

Background: Corals worldwide are in decline due to climate change effects (e.g., rising seawater temperatures), pollution, and exploitation. The ability of corals to cope with these stressors in the long run depends on the evolvability of the underlying genetic networks and proteins, which remain largely unknown. A genome-wide scan for positively selected genes between related coral species can help to narrow down the search space considerably.

Methodology/principal Findings: We screened a set of 2,604 putative orthologs from EST-based sequence datasets of the coral species Acropora millepora and Acropora palmata to determine the fraction and identity of proteins that may experience adaptive evolution. 7% of the orthologs show elevated rates of evolution. Taxonomically-restricted (i.e. lineage-specific) genes show a positive selection signature more frequently than genes that are found across many animal phyla. The class of proteins that displayed elevated evolutionary rates was significantly enriched for proteins involved in immunity and defense, reproduction, and sensory perception. We also found elevated rates of evolution in several other functional groups such as management of membrane vesicles, transmembrane transport of ions and organic molecules, cell adhesion, and oxidative stress response. Proteins in these processes might be related to the endosymbiotic relationship corals maintain with dinoflagellates in the genus Symbiodinium.

Conclusion/relevance: This study provides a birds-eye view of the processes potentially underlying coral adaptation, which will serve as a foundation for future work to elucidate the rates, patterns, and mechanisms of corals' evolutionary response to global climate change.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0020392PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3102110PMC
September 2011

Environmental barcoding reveals massive dinoflagellate diversity in marine environments.

PLoS One 2010 Nov 15;5(11):e13991. Epub 2010 Nov 15.

The Biodiversity Research Centre, University of British Columbia, Vancouver, British Columbia, Canada.

Background: Dinoflagellates are an ecologically important group of protists with important functions as primary producers, coral symbionts and in toxic red tides. Although widely studied, the natural diversity of dinoflagellates is not well known. DNA barcoding has been utilized successfully for many protist groups. We used this approach to systematically sample known "species", as a reference to measure the natural diversity in three marine environments.

Methodology/principal Findings: In this study, we assembled a large cytochrome c oxidase 1 (COI) barcode database from 8 public algal culture collections plus 3 private collections worldwide resulting in 336 individual barcodes linked to specific cultures. We demonstrate that COI can identify to the species level in 15 dinoflagellate genera, generally in agreement with existing species names. Exceptions were found in species belonging to genera that were generally already known to be taxonomically challenging, such as Alexandrium or Symbiodinium. Using this barcode database as a baseline for cultured dinoflagellate diversity, we investigated the natural diversity in three diverse marine environments (Northeast Pacific, Northwest Atlantic, and Caribbean), including an evaluation of single-cell barcoding to identify uncultivated groups. From all three environments, the great majority of barcodes were not represented by any known cultured dinoflagellate, and we also observed an explosion in the diversity of genera that previously contained a modest number of known species, belonging to Kareniaceae. In total, 91.5% of non-identical environmental barcodes represent distinct species, but only 51 out of 603 unique environmental barcodes could be linked to cultured species using a conservative cut-off based on distances between cultured species.

Conclusions/significance: COI barcoding was successful in identifying species from 70% of cultured genera. When applied to environmental samples, it revealed a massive amount of natural diversity in dinoflagellates. This highlights the extent to which we underestimate microbial diversity in the environment.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0013991PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2981561PMC
November 2010

Environmental symbiont acquisition may not be the solution to warming seas for reef-building corals.

PLoS One 2010 Oct 7;5(10):e13258. Epub 2010 Oct 7.

Graduate Program in Evolution, Ecology and Behavior, Department of Geology, University at Buffalo, Buffalo, New York, United States of America.

Background: Coral reefs worldwide are in decline. Much of the mortality can be attributed to coral bleaching (loss of the coral's intracellular photosynthetic algal symbiont) associated with global warming. How corals will respond to increasing oceanic temperatures has been an area of extensive study and debate. Recovery after a bleaching event is dependent on regaining symbionts, but the source of repopulating symbionts is poorly understood. Possibilities include recovery from the proliferation of endogenous symbionts or recovery by uptake of exogenous stress-tolerant symbionts.

Methodology/principal Findings: To test one of these possibilities, the ability of corals to acquire exogenous symbionts, bleached colonies of Porites divaricata were exposed to symbiont types not normally found within this coral and symbiont acquisition was monitored. After three weeks exposure to exogenous symbionts, these novel symbionts were detected in some of the recovering corals, providing the first experimental evidence that scleractinian corals are capable of temporarily acquiring symbionts from the water column after bleaching. However, the acquisition was transient, indicating that the new symbioses were unstable. Only those symbiont types present before bleaching were stable upon recovery, demonstrating that recovery was from the resident in situ symbiont populations.

Conclusions/significance: These findings suggest that some corals do not have the ability to adjust to climate warming by acquiring and maintaining exogenous, more stress-tolerant symbionts. This has serious ramifications for the success of coral reefs and surrounding ecosystems and suggests that unless actions are taken to reverse it, climate change will lead to decreases in biodiversity and a loss of coral reefs.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0013258PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2951366PMC
October 2010

Isolation and characterization of microsatellite loci in Symbiodinium B1/B184, the dinoflagellate symbiont of the Caribbean sea fan coral, Gorgonia ventalina.

Mol Ecol Resour 2009 May 2;9(3):989-93. Epub 2009 Mar 2.

Department of Ecology and Evolutionary Biology, Dale R. Corson Hall, Cornell University, Ithaca, NY 14853, USA, Department of Biological Sciences, 101 Life Sciences, Auburn University, Auburn, AL 36849, USA, Department of Biological Sciences, 447 Hochstetter Hall, State University of New York at Buffalo, Buffalo, NY 14260, USA.

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.
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http://dx.doi.org/10.1111/j.1755-0998.2009.02549.xDOI Listing
May 2009

The host transcriptome remains unaltered during the establishment of coral-algal symbioses.

Mol Ecol 2009 May 20;18(9):1823-33. Epub 2009 Mar 20.

School of Natural Sciences, University of California, Merced, CA 95344, USA.

Coral reefs are based on the symbiotic relationship between corals and photosynthetic dinoflagellates of the genus Symbiodinium. We followed gene expression of coral larvae of Acropora palmata and Montastraea faveolata after exposure to Symbiodinium strains that differed in their ability to establish symbioses. We show that the coral host transcriptome remains almost unchanged during infection by competent symbionts, but is massively altered by symbionts that fail to establish symbioses. Our data suggest that successful coral-algal symbioses depend mainly on the symbionts' ability to enter the host in a stealth manner rather than a more active response from the coral host.
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http://dx.doi.org/10.1111/j.1365-294X.2009.04167.xDOI Listing
May 2009

Evolutionary analysis of orthologous cDNA sequences from cultured and symbiotic dinoflagellate symbionts of reef-building corals (Dinophyceae: Symbiodinium).

Comp Biochem Physiol Part D Genomics Proteomics 2009 Jun 6;4(2):67-74. Epub 2008 Dec 6.

School of Natural Sciences, University of California, Merced, P.O. Box 2039, Merced, CA 95344, USA.

Dinoflagellates are ubiquitous marine and freshwater protists. The endosymbiotic relationship between dinoflagellates of the genus Symbiodinium (also known as zooxanthellae) and corals forms the basis of coral reefs. We constructed and analyzed a cDNA library from a cultured Symbiodinium species clade A (CassKB8). The majority of annotated ESTs from the Symbiodinium sp. CassKB8 library cover metabolic genes. Most of those belong to either carbohydrate or energy metabolism. In addition, components of extracellular signal transduction pathways and genes that play a role in cell-cell communication were identified. In a subsequent analysis, we determined all orthologous cDNA sequences between this library (1,484 unique sequences) and a library from a Symbiodinium species clade C (C3) (3,336 unique sequences) that was isolated directly from its symbiotic host. A set of 115 orthologs were identified between Symbiodinium sp. CassKB8 and Symbiodinium sp. C3. These orthologs were subdivided into three groups that show different characteristics and functions: conserved across eukaryotes (CE), dinoflagellate-specific (DS) and Symbiodinium-specific (SS). Orthologs conserved across eukaryotes are mainly comprised of housekeeping genes, photosynthesis-related transcripts and metabolic proteins, whereas the function for most of the dinoflagellate-specific orthologs remains unknown. A dN/dS analysis identified the highest ratio in a Symbiodinium-specific ortholog and evidence for positive selection in a dinoflagellate-specific gene. Evolution of genes and pathways in different dinoflagellates seems to be affected by different lifestyles, and a symbiotic lifestyle may affect population structure and strength of selection. This study is the first evolutionary comparative analysis of orthologs from two coral dinoflagellate symbionts.
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http://dx.doi.org/10.1016/j.cbd.2008.11.001DOI Listing
June 2009

Coral life history and symbiosis: functional genomic resources for two reef building Caribbean corals, Acropora palmata and Montastraea faveolata.

BMC Genomics 2008 Feb 25;9:97. Epub 2008 Feb 25.

Biology Department, Vassar College, 124 Raymond Avenue, Poughkeepsie, NY 12604, USA.

Background: Scleractinian corals are the foundation of reef ecosystems in tropical marine environments. Their great success is due to interactions with endosymbiotic dinoflagellates (Symbiodinium spp.), with which they are obligately symbiotic. To develop a foundation for studying coral biology and coral symbiosis, we have constructed a set of cDNA libraries and generated and annotated ESTs from two species of corals, Acropora palmata and Montastraea faveolata.

Results: We generated 14,588 (Ap) and 3,854 (Mf) high quality ESTs from five life history/symbiosis stages (spawned eggs, early-stage planula larvae, late-stage planula larvae either infected with symbionts or uninfected, and adult coral). The ESTs assembled into a set of primarily stage-specific clusters, producing 4,980 (Ap), and 1,732 (Mf) unigenes. The egg stage library, relative to the other developmental stages, was enriched in genes functioning in cell division and proliferation, transcription, signal transduction, and regulation of protein function. Fifteen unigenes were identified as candidate symbiosis-related genes as they were expressed in all libraries constructed from the symbiotic stages and were absent from all of the non symbiotic stages. These include several DNA interacting proteins, and one highly expressed unigene (containing 17 cDNAs) with no significant protein-coding region. A significant number of unigenes (25) encode potential pattern recognition receptors (lectins, scavenger receptors, and others), as well as genes that may function in signaling pathways involved in innate immune responses (toll-like signaling, NFkB p105, and MAP kinases). Comparison between the A. palmata and an A. millepora EST dataset identified ferritin as a highly expressed gene in both datasets that appears to be undergoing adaptive evolution. Five unigenes appear to be restricted to the Scleractinia, as they had no homology to any sequences in the nr databases nor to the non-scleractinian cnidarians Nematostella vectensis and Hydra magnipapillata.

Conclusion: Partial sequencing of 5 cDNA libraries each for A. palmata and M. faveolata has produced a rich set of candidate genes (4,980 genes from A. palmata, and 1,732 genes from M. faveolata) that we can use as a starting point for examining the life history and symbiosis of these two species, as well as to further expand the dataset of cnidarian genes for comparative genomics and evolutionary studies.
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http://dx.doi.org/10.1186/1471-2164-9-97DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2291459PMC
February 2008

Stable Symbiodinium composition in the sea fan Gorgonia ventalina during temperature and disease stress.

Biol Bull 2005 Dec;209(3):227-34

Department of Biological Sciences, 109 Cooke Hall, University at Buffalo (State University of New York), Buffalo, New York 14260, USA.

Like most Caribbean octocorals, Gorgonia ventalina, the common sea fan, harbors endosymbiotic dinoflagellates belonging to the genus Symbiodinium. When stressed, the host can lose these algal symbionts, a phenomenon termed "bleaching." Many cnidarians host multiple types of algal symbionts within the genus Symbiodinium, and certain types of algae may be more tolerant of stress than others. We examined the effects of temperature, temperature-induced bleaching, and infection by Aspergillus sydowii, a fungal pathogen, on Symbiodinium types harbored by the sea fan Gorgonia ventalina in the Florida Keys. Symbiont type, identified on the basis of variation in small subunit nuclear ribosomal genes or large subunit chloroplast ribosomal genes, did not vary with temperature treatment or infection status. Although allelic variation based on one microsatellite locus was found among samples and reef site, it did not consistently correlate with temperature, treatment, or disease status, suggesting that the symbiont-host relationship is stable. An aberrant PCR product was found in samples collected at one site and could be used to differentiate Symbiodinium populations among sites in the Florida Keys.
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http://dx.doi.org/10.2307/3593112DOI Listing
December 2005

The acquisition of exogenous algal symbionts by an octocoral after bleaching.

Science 2004 Jun;304(5676):1490-2

Department of Biological Sciences, State University of New York at Buffalo, Buffalo, NY 14260, USA.

Episodes of coral bleaching (loss of the symbiotic dinoflagellates) and coral mortality have occurred with increasing frequency over the past two decades. Although some corals recover from bleaching events, the source of the repopulating symbionts is unknown. Here we show that after bleaching, the adult octocoral Briareum sp. acquire dinoflagellate symbionts (Symbiodinium sp.) from the environment. Uptake of exogenous symbionts provides a mechanism for response to changes in the environment and resilience in the symbiosis.
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http://dx.doi.org/10.1126/science.1097323DOI Listing
June 2004

Molecular characterization of nuclear small subunit (18S)-rDNA pseudogenes in a symbiotic dinoflagellate (Symbiodinium, Dinophyta).

J Eukaryot Microbiol 2003 Nov-Dec;50(6):417-21

Department of Biological Sciences, State University of New York at Buffalo, Buffalo, New York 14260-1300, USA.

For the dinoflagellates, an important group of single-cell protists, some nuclear rDNA phylogenetic studies have reported the discovery of rDNA pseudogenes. However, it is unknown if these aberrant molecules are confined to free-living taxa or occur in other members of the group. We have cultured a strain of symbiotic dinoflagellate, belonging to the genus Symbiodinium, which produces three distinct amplicons following PCR for nuclear small subunit (18S) rDNA genes. These amplicons contribute to a unique restriction fragment length polymorphism pattern diagnostic for this particular strain. Sequence analyses revealed that the largest amplicon was the expected region of 18S-rDNA, while the two smaller amplicons are Symbiodinium nuclear 18S-rDNA genes that contain single long tracts of nucleotide deletions. Reverse transcription (RT)-PCR experiments did not detect RNA transcripts of these latter genes, suggesting that these molecules represent the first report of nuclear 18S-rDNA pseudogenes from the genome of Symbiodinium. As in the free-living dinoflagellates, nuclear rDNA pseudogenes are effective indicators of unique Symbiodinium strains. Furthermore, the evolutionary pattern of dinoflagellate nuclear rDNA pseudogenes appears to be unique among organisms studied to date, and future studies of these unusual molecules will provide insight on the cellular biology and genomic evolution of these protists.
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http://dx.doi.org/10.1111/j.1550-7408.2003.tb00264.xDOI Listing
March 2004

Phylogenetic identification of symbiotic dinoflagellates via length heteroplasmy in domain V of chloroplast large subunit (cp23S)-ribosomal DNA sequences.

Mar Biotechnol (NY) 2003 Mar-Apr;5(2):130-40

Department of Biological Science, State University of New York at Buffalo, Buffalo, NY 14260-1300, USA.

A protocol that takes advantage of length heteroplasmy in domain V of chloroplast large subunit (cp23S)-ribosomal DNA to identify members of the symbiotic dinoflagellate genus Symbiodinium is presented. This protocol is highly specific for Symbiodinium, can provide intercladal and intracladal identification of a particular Symbiodinium isolate, and can detect multiple Symbiodinium chloroplast genotypes simultaneously in the same isolate, making his technique attractive for a variety of research questions. We used this technique to characterize variation among Symbiodinium populations associated with a range of phylogenetically diverse and geographically discrete hosts. We also examined symbiont variation within a single host, the Caribbean gorgonian Pseudopterogorgia elisabethae, from 9 sites in the Bahamas, and we report a previously undocumented level of symbiont specificity for particular members of Symbiodinium clade B in this gorgonian.
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http://dx.doi.org/10.1007/s10126-002-0076-zDOI Listing
August 2003

Molecular genetic evidence that dinoflagellates belonging to the genus Symbiodinium freudenthal are haploid.

Biol Bull 2003 Feb;204(1):10-20

Department of Biological Science, State University of New York at Buffalo, Buffalo, New York 14260-1300, USA.

Microscopic and cytological evidence suggest that many dinoflagellates possess a haploid nuclear phase. However, the ploidy of a number of dinoflagellates remains unknown, and molecular genetic support for haploidy in this group has been lacking. To elucidate the ploidy of symbiotic dinoflagellates belonging to the genus Symbiodinium, we used five polymorphic microsatellites to examine populations harbored by the Caribbean gorgonians Plexaura kuna and Pseudopterogorgia elisabethae; we also studied a series of Symbiodinium cultures. In 690 out of 728 Symbiodinium samples in hospite (95% of the cases) and in all 45 Symbiodinium cultures, only a single allele was recovered per locus. Statistical testing of the Symbiodinium populations harbored by P. elisabethae revealed that the observed genotype frequencies deviate significantly from those expected under Hardy-Weinberg equilibrium. Taken together, our results confirm that, in the vegetative life stage, members of Symbiodinium, both cultured and in hospite, are haploid. Furthermore, based on the phylogenetics of the dinoflagellates, haploidy in vegetative cells appears to be an ancestral trait that extends to all 2,000 extant species of these important unicellular protists.
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http://dx.doi.org/10.2307/1543491DOI Listing
February 2003

Molecular phylogeny of symbiotic dinoflagellates inferred from partial chloroplast large subunit (23S)-rDNA sequences.

Mol Phylogenet Evol 2002 May;23(2):97-111

Department of Biological Sciences, State University of New York at Buffalo, Buffalo, NY 14260-1300, USA.

Symbiotic associations between invertebrates and dinoflagellates of the genus Symbiodinium are a common occurrence in marine environments. However, despite our extensive knowledge concerning the physiological contributions of these algae to their symbiotic partners, our understanding of zooxanthella phylogenetics is still in its early stages. In the past 10 years, studies of Symbiodinium phylogenetics have relied solely on nuclear ribosomal (rDNA) genes. To date, organellar DNA sequences have not been employed to infer phylogenies for this genus of symbiotic dinoflagellates. We address this by presenting the first Symbiodinium phylogeny based on chloroplast (cp) large subunit (23S)-rDNA sequences. Cp23S-rDNA Domain V sequences were determined for 35 dinoflagellate cultures isolated from a range of invertebrate host species and geographical locations. Symbiodinium phylogenies inferred from cp23S-rDNA produced topologies that were not statistically different from those generated from nuclear rDNA, providing the first independent evidence supporting the published major clades of Symbiodinium. In addition, comparisons of sequence dissimilarity indicated that cp23S-rDNA Domain V evolves 9-30 times faster than the V1-V4 regions of nuclear small subunit (n18S)-rDNA, 1-7 times as fast as the D1-D3 regions of nuclear large subunit (n28S)-rDNA, and 0.27-2.25 times that of the internal transcribed spacer (ITS)-rDNA region. Our data suggested that cp23S-rDNA Domain V will prove to be a useful molecule for exploring Symbiodinium phylogenetics.
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http://dx.doi.org/10.1016/S1055-7903(02)00010-6DOI Listing
May 2002

POPULATION STRUCTURE OF A CLONAL GORGONIAN CORAL: THE INTERPLAY BETWEEN CLONAL REPRODUCTION AND DISTURBANCE.

Evolution 1998 Apr;52(2):379-393

Department of Biological Sciences, State University of New York at Buffalo, Buffalo, New York, 14260.

Clonality is a common feature of plants and benthic marine organisms. In some cases clonal propagation results in a modest increase in population density, while in other cases dense populations may be generated by the propagation of only a few clones. We analyzed the population structure of the clonal gorgonian Plexaura kuna across several reef habitats with a range of disturbance regimes in the San Blas Islands, Panama, and the Florida Keys, U.S.A. Using multilocus DNA fingerprinting to distinguish clones, we estimated that clones ranged in size from single individuals to 500 colonies. The number of genotypes identified on nine reefs ranged from three to 25. Population density and clonal structure varied markedly among reefs with G :G ranging from 0.03 to 1.00. On some reefs vegetative reproduction transformed P. kuna from a rare species to the numerically most abundant gorgonian. The effect of clonal propagation on P. kuna population structure was dependent on interactions between fragmentation and the reef environment (disturbance regime, substratum). We present a generalized model relating population structure of clonal species to disturbance and the mode of vegetative propagation. Disturbance promotes colony propagation and skews the size-frequency distribution of clones among P. kuna and many species that propagate via fragmentation. Propagation of these species is promoted by disturbance (disturbance sensitive), and they tend to have clones that are dispersed across local sites. Species that fragment and have dispersed clones, have high genotypic diversity in habitats with low levels of disturbance. Genotypic diversity then decreases at intermediate disturbance and increases again at the highest disturbance levels. Clonal species that do not rely on disturbance for vegetative propagation (disturbance insensitive) generally do not disperse and form aggregated clones. Among these taxa disturbance has a greater affect on individual survival than on propagation. Genotypic diversity is directly related to the level of disturbance until very high levels of disturbance, at which time genotypic diversity declines.
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http://dx.doi.org/10.1111/j.1558-5646.1998.tb01639.xDOI Listing
April 1998
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