Now showing items 41-60 of 113

    • Evidence for a role of viruses in the thermal sensitivity of coral photosymbionts

      Levin, Rachel Ashley; Voolstra, Christian R.; Weynberg, Karen Dawn; Oppen, Madeleine Josephine Henriette van (The ISME Journal, Springer Nature, 2016-12-02) [Article]
      Symbiodinium, the dinoflagellate photosymbiont of corals, is posited to become more susceptible to viral infections when heat-stressed. To investigate this hypothesis, we mined transcriptome data of a thermosensitive and a thermotolerant type C1 Symbiodinium population at ambient (27 °C) and elevated (32°C) temperatures. We uncovered hundreds of transcripts from nucleocytoplasmic large double-stranded DNA viruses (NCLDVs) and the genome of a novel positive-sense single-stranded RNA virus (+ssRNAV). In the transcriptome of the thermosensitive population only, +ssRNAV transcripts had remarkable expression levels in the top 0.03% of all transcripts at 27 °C, but at 32 °C, expression levels of +ssRNAV transcripts decreased, while expression levels of anti-viral transcripts increased. In both transcriptomes, expression of NCLDV transcripts increased at 32 °C, but thermal induction of NCLDV transcripts involved in DNA manipulation was restricted to the thermosensitive population. Our findings reveal that viruses infecting Symbiodinium are affected by heat stress and may contribute to Symbiodinium thermal sensitivity.
    • Distinct Bacterial Communities Associated with the Coral Model Aiptasia in Aposymbiotic and Symbiotic States with Symbiodinium

      Röthig, Till; Martins Da Costa, Ruben; Simona, Fabia; Baumgarten, Sebastian; Torres, Ana F.; Radhakrishnan, Anand; Aranda, Manuel; Voolstra, Christian R. (Frontiers in Marine Science, Frontiers Media SA, 2016-11-18) [Article]
      Coral reefs are in decline. The basic functional unit of coral reefs is the coral metaorganism or holobiont consisting of the cnidarian host animal, symbiotic algae of the genus Symbiodinium, and a specific consortium of bacteria (among others), but research is slow due to the difficulty of working with corals. Aiptasia has proven to be a tractable model system to elucidate the intricacies of cnidarian-dinoflagellate symbioses, but characterization of the associated bacterial microbiome is required to provide a complete and integrated understanding of holobiont function. In this work, we characterize and analyze the microbiome of aposymbiotic and symbiotic Aiptasia and show that bacterial associates are distinct in both conditions. We further show that key microbial associates can be cultured without their cnidarian host. Our results suggest that bacteria play an important role in the symbiosis of Aiptasia with Symbiodinium, a finding that underlines the power of the Aiptasia model system where cnidarian hosts can be analyzed in aposymbiotic and symbiotic states. The characterization of the native microbiome and the ability to retrieve culturable isolates contributes to the resources available for the Aiptasia model system. This provides an opportunity to comparatively analyze cnidarian metaorganisms as collective functional holobionts and as separated member species. We hope that this will accelerate research into understanding the intricacies of coral biology, which is urgently needed to develop strategies to mitigate the effects of environmental change.
    • Year-Long Monitoring of Physico-Chemical and Biological Variables Provide a Comparative Baseline of Coral Reef Functioning in the Central Red Sea

      Roik, Anna Krystyna; Röthig, Till; Roder, Cornelia; Ziegler, Maren; Kremb, Stephan Georg; Voolstra, Christian R. (PLOS ONE, Public Library of Science (PLoS), 2016-11-09) [Article]
      Coral reefs in the central Red Sea are sparsely studied and in situ data on physico-chemical and key biotic variables that provide an important comparative baseline are missing. To address this gap, we simultaneously monitored three reefs along a cross-shelf gradient for an entire year over four seasons, collecting data on currents, temperature, salinity, dissolved oxygen (DO), chlorophyll-a, turbidity, inorganic nutrients, sedimentation, bacterial communities of reef water, and bacterial and algal composition of epilithic biofilms. Summer temperature (29–33°C) and salinity (39 PSU) exceeded average global maxima for coral reefs, whereas DO concentration was low (2–4 mg L-1). While temperature and salinity differences were most pronounced between seasons, DO, chlorophyll-a, turbidity, and sedimentation varied most between reefs. Similarly, biotic communities were highly dynamic between reefs and seasons. Differences in bacterial biofilms were driven by four abundant families: Rhodobacteraceae, Flavobacteriaceae, Flammeovirgaceae, and Pseudanabaenaceae. In algal biofilms, green crusts, brown crusts, and crustose coralline algae were most abundant and accounted for most of the variability of the communities. Higher bacterial diversity of biofilms coincided with increased algal cover during spring and summer. By employing multivariate matching, we identified temperature, salinity, DO, and chlorophyll-a as the main contributing physico-chemical drivers of biotic community structures. These parameters are forecast to change most with the progression of ocean warming and increased nutrient input, which suggests an effect on the recruitment of Red Sea benthic communities as a result of climate change and anthropogenic influence. In conclusion, our study provides insight into coral reef functioning in the Red Sea and a comparative baseline to support coral reef studies in the region.
    • Sex Change in Clownfish: Molecular Insights from Transcriptome Analysis

      Castano, Laura Casas; Saborido-Rey, Fran; Ryu, Tae Woo; Michell, Craig; Ravasi, Timothy; Irigoien, Xabier (Scientific Reports, Springer Nature, 2016-10-17) [Article]
      Sequential hermaphroditism is a unique reproductive strategy among teleosts that is displayed mainly in fish species living in the coral reef environment. The reproductive biology of hermaphrodites has long been intriguing; however, very little is known about the molecular pathways underlying their sex change. Here, we provide the first de novo transcriptome analyses of a hermaphrodite teleost´s undergoing sex change in its natural environment. Our study has examined relative gene expression across multiple groups—rather than just two contrasting conditions— and has allowed us to explore the differential expression patterns throughout the whole process. Our analysis has highlighted the rapid and complex genomic response of the brain associated with sex change, which is subsequently transmitted to the gonads, identifying a large number of candidate genes, some well-known and some novel, involved in the process. The present study provides strong evidence of the importance of the sex steroidogenic machinery during sex change in clownfish, with the aromatase gene playing a central role, both in the brain and the gonad. This work constitutes the first genome-wide study in a social sex-changing species and provides insights into the genetic mechanism governing social sex change and gonadal restructuring in protandrous hermaphrodites.
    • Recent origin and semi-permeable species boundaries in the scleractinian coral genus Stylophora from the Red Sea

      Arrigoni, Roberto; Benzoni, Francesca; Terraneo, Tullia Isotta; Caragnano, Annalisa; Berumen, Michael L. (Scientific Reports, Springer Nature, 2016-10-07) [Article]
      Reticulate evolution, introgressive hybridisation, and phenotypic plasticity have been documented in scleractinian corals and have challenged our ability to interpret speciation processes. Stylophora is a key model system in coral biology and physiology, but genetic analyses have revealed that cryptic lineages concealed by morphological stasis exist in the Stylophora pistillata species complex. The Red Sea represents a hotspot for Stylophora biodiversity with six morphospecies described, two of which are regionally endemic. We investigated Stylophora species boundaries from the Red Sea and the associated Symbiodinium by sequencing seven DNA loci. Stylophora morphospecies from the Red Sea were not resolved based on mitochondrial phylogenies and showed nuclear allele sharing. Low genetic differentiation, weak isolation, and strong gene flow were found among morphospecies although no signals of genetic recombination were evident among them. Stylophora mamillata harboured Symbiodinium clade C whereas the other two Stylophora morphospecies hosted either Symbiodinium clade A or C. These evolutionary patterns suggest that either gene exchange occurs through reticulate evolution or that multiple ecomorphs of a phenotypically plastic species occur in the Red Sea. The recent origin of the lineage leading to the Red Sea Stylophora may indicate an ongoing speciation driven by environmental changes and incomplete lineage sorting.
    • Aiptasia sp. larvae as a model to reveal mechanisms of symbiont selection in cnidarians

      Wolfowicz, Iliona; Baumgarten, Sebastian; Voss, Philipp A.; Hambleton, Elizabeth A.; Voolstra, Christian R.; Hatta, Masayuki; Guse, Annika (Scientific Reports, Springer Nature, 2016-09-01) [Article]
      Symbiosis, defined as the persistent association between two distinct species, is an evolutionary and ecologically critical phenomenon facilitating survival of both partners in diverse habitats. The biodiversity of coral reef ecosystems depends on a functional symbiosis with photosynthetic dinoflagellates of the highly diverse genus Symbiodinium, which reside in coral host cells and continuously support their nutrition. The mechanisms underlying symbiont selection to establish a stable endosymbiosis in non-symbiotic juvenile corals are unclear. Here we show for the first time that symbiont selection patterns for larvae of two Acropora coral species and the model anemone Aiptasia are similar under controlled conditions. We find that Aiptasia larvae distinguish between compatible and incompatible symbionts during uptake into the gastric cavity and phagocytosis. Using RNA-Seq, we identify a set of candidate genes potentially involved in symbiosis establishment. Together, our data complement existing molecular resources to mechanistically dissect symbiont phagocytosis in cnidarians under controlled conditions, thereby strengthening the role of Aiptasia larvae as a powerful model for cnidarian endosymbiosis establishment.
    • Draft genome of an iconic Red Sea reef fish, the blacktail butterflyfish (Chaetodon austriacus): current status and its characteristics

      DiBattista, Joseph; Wang, Xin; Saenz Agudelo, Pablo; Piatek, Marek J.; Aranda, Manuel; Berumen, Michael L. (Molecular Ecology Resources, Wiley, 2016-08-29) [Article]
      Butterflyfish are among the most iconic of the coral reef fishes and represent a model system to study general questions of biogeography, evolution and population genetics. We assembled and annotated the genome sequence of the blacktail butterflyfish (Chaetodon austriacus), an Arabian region endemic species that is reliant on coral reefs for food and shelter. Using available bony fish (superclass Osteichthyes) genomes as a reference, a total of 28 926 high-quality protein-coding genes were predicted from 13 967 assembled scaffolds. The quality and completeness of the draft genome of C. austriacus suggest that it has the potential to serve as a resource for studies on the co-evolution of reef fish adaptations to the unique Red Sea environment, as well as a comparison of gene sequences between closely related congeneric species of butterflyfish distributed more broadly across the tropical Indo-Pacific. © 2016 John Wiley & Sons Ltd.
    • Diversity and function of prevalent symbiotic marine bacteria in the genus Endozoicomonas

      Neave, Matthew J.; Apprill, Amy; Ferrier-Pagès, Christine; Voolstra, Christian R. (Applied Microbiology and Biotechnology, Springer Nature, 2016-08-24) [Article]
      Endozoicomonas bacteria are emerging as extremely diverse and flexible symbionts of numerous marine hosts inhabiting oceans worldwide. Their hosts range from simple invertebrate species, such as sponges and corals, to complex vertebrates, such as fish. Although widely distributed, the functional role of Endozoicomonas within their host microenvironment is not well understood. In this review, we provide a summary of the currently recognized hosts of Endozoicomonas and their global distribution. Next, the potential functional roles of Endozoicomonas, particularly in light of recent microscopic, genomic, and genetic analyses, are discussed. These analyses suggest that Endozoicomonas typically reside in aggregates within host tissues, have a free-living stage due to their large genome sizes, show signs of host and local adaptation, participate in host-associated protein and carbohydrate transport and cycling, and harbour a high degree of genomic plasticity due to the large proportion of transposable elements residing in their genomes. This review will finish with a discussion on the methodological tools currently employed to study Endozoicomonas and host interactions and review future avenues for studying complex host-microbial symbioses.
    • Molecular signatures of transgenerational response to ocean acidification in a species of reef fish

      Schunter, Celia Marei; Welch, Megan J.; Ryu, Tae Woo; Zhang, Huoming; Berumen, Michael L.; Nilsson, Göran E.; Munday, Philip L.; Ravasi, Timothy (Nature Climate Change, Springer Nature, 2016-08-01) [Article]
      The impact of ocean acidification on marine ecosystems will depend on species capacity to adapt. Recent studies show that the behaviour of reef fishes is impaired at projected CO levels; however, individual variation exists that might promote adaptation. Here, we show a clear signature of parental sensitivity to high CO in the brain molecular phenotype of juvenile spiny damselfish, Acanthochromis polyacanthus, primarily driven by circadian rhythm genes. Offspring of CO -tolerant and CO -sensitive parents were reared at near-future CO (754 μatm) or present-day control levels (414 μatm). By integrating 33 brain transcriptomes and proteomes with a de novo assembled genome we investigate the molecular responses of the fish brain to increased CO and the expression of parental tolerance to high CO in the offspring molecular phenotype. Exposure to high CO resulted in differential regulation of 173 and 62 genes and 109 and 68 proteins in the tolerant and sensitive groups, respectively. Importantly, the majority of differences between offspring of tolerant and sensitive parents occurred in high CO conditions. This transgenerational molecular signature suggests that individual variation in CO sensitivity could facilitate adaptation of fish populations to ocean acidification.
    • Differential specificity between closely related corals and abundant Endozoicomonas endosymbionts across global scales

      Neave, Matthew J.; Rachmawati, Rita; Xun, Liping; Michell, Craig; Bourne, David G; Apprill, Amy; Voolstra, Christian R. (The ISME Journal, Springer Nature, 2016-07-08) [Article]
      Reef-building corals are well regarded not only for their obligate association with endosymbiotic algae, but also with prokaryotic symbionts, the specificity of which remains elusive. To identify the central microbial symbionts of corals, their specificity across species and conservation over geographic regions, we sequenced partial SSU ribosomal RNA genes of Bacteria and Archaea from the common corals Stylophora pistillata and Pocillopora verrucosa across 28 reefs within seven major geographical regions. We demonstrate that both corals harbor Endozoicomonas bacteria as their prevalent symbiont. Importantly, catalyzed reporter deposition–fluorescence in situ hybridization (CARD–FISH) with Endozoicomonas-specific probes confirmed their residence as large aggregations deep within coral tissues. Using fine-scale genotyping techniques and single-cell genomics, we demonstrate that P. verrucosa harbors the same Endozoicomonas, whereas S. pistillata associates with geographically distinct genotypes. This specificity may be shaped by the different reproductive strategies of the hosts, potentially uncovering a pattern of symbiont selection that is linked to life history. Spawning corals such as P. verrucosa acquire prokaryotes from the environment. In contrast, brooding corals such as S. pistillata release symbiont-packed planula larvae, which may explain a strong regional signature in their microbiome. Our work contributes to the factors underlying microbiome specificity and adds detail to coral holobiont functioning.
    • Species delimitation in the coral genus Goniopora (Scleractinia, Poritidae) from the Saudi Arabian Red Sea

      Terraneo, Tullia Isotta; Benzoni, Francesca; Arrigoni, Roberto; Berumen, Michael L. (Molecular Phylogenetics and Evolution, Elsevier BV, 2016-06-19) [Article]
      Variable skeletal morphology, genotype induced plasticity, and homoplasy of skeletal structures have presented major challenges for scleractinian coral taxonomy and systematics since the 18th century. Although the recent integration of genetic and micromorphological data is helping to clarify the taxonomic confusion within the order, phylogenetic relationships and species delimitation within most coral genera are still far from settled. In the present study, the species boundaries in the scleractinian coral genus Goniopora were investigated using 199 colonies from the Saudi Arabian Red Sea and sequencing of four molecular markers: the mitochondrial intergenic spacer between CytB and NAD2, the nuclear ribosomal ITS region, and two single-copy nuclear genes (ATPsβ and CalM). DNA sequence data were analyzed using a variety of methods and exploratory species-delimitation tools. The results were broadly congruent in identifying five distinct molecular lineages within the sequenced Goniopora samples: G. somaliensis/G. savignyi, G. djiboutiensis/G. lobata, G. stokesi, G. albiconus/G. tenuidens, and G. minor/G. gracilis. Although the traditional macromorphological characters used to identify these nine morphospecies were not able to discriminate the obtained molecular clades, informative micromorphological and microstructural features (such as the micro-ornamentation and the arrangement of the columella) were recovered among the five lineages. Moreover, unique in vivo morphologies were associated with the genetic-delimited lineages, further supporting the molecular findings. This study represents the first attempt to identify species boundaries within Goniopora using a combined morpho-molecular approach. The obtained data establish a basis for future taxonomic revision of the genus, which should include colonies across its entire geographical distribution in the Indo-Pacific.
    • Comparative genomics explains the evolutionary success of reef-forming corals

      Bhattacharya, Debashish; Agrawal, Shobhit; Aranda, Manuel; Baumgarten, Sebastian; Belcaid, Mahdi; Drake, Jeana L; Erwin, Douglas; Foret, Sylvian; Gates, Ruth D; Gruber, David F; Kamel, Bishoy; Lesser, Michael P; Levy, Oren; Liew, Yi Jin; MacManes, Matthew; Mass, Tali; Medina, Monica; Mehr, Shaadi; Meyer, Eli; Price, Dana C; Putnam, Hollie M; Qiu, Huan; Shinzato, Chuya; Shoguchi, Eiichi; Stokes, Alexander J; Tambutté, Sylvie; Tchernov, Dan; Voolstra, Christian R.; Wagner, Nicole; Walker, Charles W; Weber, Andreas PM; Weis, Virginia; Zelzion, Ehud; Zoccola, Didier; Falkowski, Paul G (eLife, eLife Sciences Publications, Ltd, 2016-05-24) [Article]
      Transcriptome and genome data from twenty stony coral species and a selection of reference bilaterians were studied to elucidate coral evolutionary history. We identified genes that encode the proteins responsible for the precipitation and aggregation of the aragonite skeleton on which the organisms live, and revealed a network of environmental sensors that coordinate responses of the host animals to temperature, light, and pH. Furthermore, we describe a variety of stress-related pathways, including apoptotic pathways that allow the host animals to detoxify reactive oxygen and nitrogen species that are generated by their intracellular photosynthetic symbionts, and determine the fate of corals under environmental stress. Some of these genes arose through horizontal gene transfer and comprise at least 0.2% of the animal gene inventory. Our analysis elucidates the evolutionary strategies that have allowed symbiotic corals to adapt and thrive for hundreds of millions of years.
    • Surgeons and suture zones: Hybridization among four surgeonfish species in the Indo-Pacific with variable evolutionary outcomes

      DiBattista, Joseph; Whitney, Jonathan; Craig, Matthew T.; Hobbs, Jean-Paul A.; Rocha, Luiz A.; Feldheim, Kevin A.; Berumen, Michael L.; Bowen, Brian W. (Molecular Phylogenetics and Evolution, Elsevier BV, 2016-05-01) [Article]
      Closely related species can provide valuable insights into evolutionary processes through comparison of their ecology, geographic distribution and the history recorded in their genomes. In the Indo-Pacific, many reef fishes are divided into sister species that come into secondary contact at biogeographic borders, most prominently where Indian Ocean and Pacific Ocean faunas meet. It is unclear whether hybridization in this contact zone represents incomplete speciation, secondary contact, an evolutionary dead-end (for hybrids) or some combination of the above. To address these issues, we conducted comprehensive surveys of two widely-distributed surgeonfish species, Acanthurus leucosternon (N = 141) and A. nigricans (N = 412), with mtDNA cytochrome b sequences and ten microsatellite loci. These surgeonfishes are found primarily in the Indian and Pacific Oceans, respectively, but overlap at the Christmas and Cocos-Keeling Islands hybrid zone in the eastern Indian Ocean. We also sampled the two other Pacific members of this species complex, A. achilles (N = 54) and A. japonicus (N = 49), which are known to hybridize with A. nigricans where their ranges overlap. Our results indicate separation between the four species that range from the recent Pleistocene to late Pliocene (235,000 to 2.25 million years ago). The Pacific A. achilles is the most divergent (and possibly ancestral) species with mtDNA dcorr ≈ 0.04, whereas the other two Pacific species (A. japonicus and A. nigricans) are distinguishable only at a population or subspecies level (ΦST = 0.6533, P < 0.001). Little population structure was observed within species, with evidence of recent population expansion across all four geographic ranges. We detected sharing of mtDNA haplotypes between species and extensive hybridization based on microsatellites, consistent with later generation hybrids but also the effects of allele homoplasy. Despite extensive introgression, 98% of specimens had concordance between mtDNA lineage and species identification based on external morphology, indicating that species integrity may not be eroding. The A. nigricans complex demonstrates a range of outcomes from incomplete speciation to secondary contact to decreasing hybridization with increasing evolutionary depth.
    • Please mind the gap – Visual census and cryptic biodiversity assessment at central Red Sea coral reefs

      Pearman, John K.; Anlauf, Holger; Irigoien, Xabier; Carvalho, Susana (Marine Environmental Research, Elsevier BV, 2016-04-28) [Article]
      Coral reefs harbor the most diverse assemblages in the ocean, however, a large proportion of the diversity is cryptic and, therefore, undetected by standard visual census techniques. Cryptic and exposed communities differ considerably in species composition and ecological function. This study compares three different coral reef assessment protocols: i) visual benthic reef surveys: ii) visual census of Autonomous Reef Monitoring Structures (ARMS) plates; and iii) metabarcoding techniques of the ARMS (including sessile, 106–500 μm and 500–2000 μm size fractions), that target the cryptic and exposed communities of three reefs in the central Red Sea. Visual census showed a dominance of Cnidaria (Anthozoa) and Rhodophyta on the reef substrate, while Porifera, Bryozoa and Rhodophyta were the most abundant groups on the ARMS plates. Metabarcoding, targeting the 18S rRNA gene, significantly increased estimates of the species diversity (p < 0.001); revealing that Annelida were generally the dominant phyla (in terms of reads) of all fractions and reefs. Furthermore, metabarcoding detected microbial eukaryotic groups such as Syndiniophyceae, Mamiellophyceae and Bacillariophyceae as relevant components of the sessile fraction. ANOSIM analysis showed that the three reef sites showed no differences based on the visual census data. Metabarcoding showed a higher sensitivity for identifying differences between reef communities at smaller geographic scales than standard visual census techniques as significant differences in the assemblages were observed amongst the reefs. Comparison of the techniques showed no similar patterns for the visual techniques while the metabarcoding of the ARMS showed similar patterns amongst fractions. Establishing ARMS as a standard tool in reef monitoring will not only advance our understanding of local processes and ecological community response to environmental changes, as different faunal components will provide complementary information but also improve the estimates of biodiversity in coral reef benthic communities. This study lays the foundations for further studies looking at integrating traditional reef survey methodologies with complementary approaches, such as metabarcoding, which investigate other components of the reef community.
    • Regal phylogeography: Range-wide survey of the marine angelfish Pygoplites diacanthus reveals evolutionary partitions between the Red Sea, Indian Ocean, and Pacific Ocean

      Coleman, Richard R.; Eble, Jeffrey A.; DiBattista, Joseph; Rocha, Luiz A.; Randall, John E.; Berumen, Michael L.; Bowen, Brian W. (Molecular Phylogenetics and Evolution, Elsevier BV, 2016-04-10) [Article]
      The regal angelfish (Pygoplites diacanthus; family Pomacanthidae) occupies reefs from the Red Sea to the central Pacific, with an Indian Ocean/Rea Sea color morph distinct from a Pacific Ocean morph. To assess population differentiation and evaluate the possibility of cryptic evolutionary partitions in this monotypic genus, we surveyed mtDNA cytochrome b and two nuclear introns (S7 and RAG2) in 547 individuals from 15 locations. Phylogeographic analyses revealed four mtDNA lineages (d = 0.006 – 0.015) corresponding to the Pacific Ocean, the Red Sea, and two admixed lineages in the Indian Ocean, a pattern consistent with known biogeographical barriers. Christmas Island in the eastern Indian Ocean had both Indian and Pacific lineages. Both S7 and RAG2 showed strong population-level differentiation between the Red Sea, Indian Ocean, and Pacific Ocean (ΦST = 0.066 – 0.512). The only consistent population sub-structure within these three regions was at the Society Islands (French Polynesia), where surrounding oceanographic conditions may reinforce isolation. Coalescence analyses indicate the Pacific (1.7 Ma) as the oldest extant lineage followed by the Red Sea lineage (1.4 Ma). Results from a median-joining network suggest radiations of two lineages from the Red Sea that currently occupy the Indian Ocean (0.7 – 0.9 Ma). Persistence of a Red Sea lineage through Pleistocene glacial cycles suggests a long-term refuge in this region. The affiliation of Pacific and Red Sea populations, apparent in cytochrome b and S7 (but equivocal in RAG2) raises the hypthosis that the Indian Ocean was recolonized from the Red Sea, possibly more than once. Assessing the genetic architecture of this widespread monotypic genus reveals cryptic evolutionary diversity that merits subspecific recognition.
    • Ancestral genetic diversity associated with the rapid spread of stress-tolerant coral symbionts in response to Holocene climate change

      Hume, Benjamin C. C.; Voolstra, Christian R.; Arif, Chatchanit; D’Angelo, Cecilia; Burt, John A.; Eyal, Gal; Loya, Yossi; Wiedenmann, Jörg (Proceedings of the National Academy of Sciences, Proceedings of the National Academy of Sciences, 2016-04-04) [Article]
      Coral communities in the Persian/Arabian Gulf (PAG) withstand unusually high salinity levels and regular summer temperature maxima of up to ∼35 °C that kill conspecifics elsewhere. Due to the recent formation of the PAG and its subsequent shift to a hot climate, these corals have had only <6, 000 y to adapt to these extreme conditions and can therefore inform on how coral reefs may respond to global warming. One key to coral survival in the world's warmest reefs are symbioses with a newly discovered alga, Symbiodinium thermophilum. Currently, it is unknown whether this symbiont originated elsewhere or emerged from unexpectedly fast evolution catalyzed by the extreme environment. Analyzing genetic diversity of symbiotic algae across >5, 000 km of the PAG, the Gulf of Oman, and the Red Sea coastline, we show that S. thermophilum is a member of a highly diverse, ancient group of symbionts cryptically distributed outside the PAG. We argue that the adjustment to temperature extremes by PAG corals was facilitated by the positive selection of preadapted symbionts. Our findings suggest that maintaining the largest possible pool of potentially stress-tolerant genotypes by protecting existing biodiversity is crucial to promote rapid adaptation to present-day climate change, not only for coral reefs, but for ecosystems in general.
    • Phylogenetic Diversity, Distribution, and Cophylogeny of Giant Bacteria (Epulopiscium) with their Surgeonfish Hosts in the Red Sea

      Miyake, Sou; Ngugi, David; Stingl, Ulrich (Frontiers in Microbiology, Frontiers Media SA, 2016-03-14) [Article]
      Epulopiscium is a group of giant bacteria found in high abundance in intestinal tracts of herbivorous surgeonfish. Despite their peculiarly large cell size (can be up to 600 μm), extreme polyploidy (some with over 100,000 genome copies per cell) and viviparity (whereby mother cells produce live offspring), details about their diversity, distribution or their role in the host gut are lacking. Previous studies have highlighted the existence of morphologically distinct Epulopiscium cell types (defined as morphotypes A to J) in some surgeonfish genera, but the corresponding genetic diversity and distribution among other surgeonfishes remain mostly unknown. Therefore, we investigated the phylogenetic diversity of Epulopiscium, distribution and co-occurrence in multiple hosts. Here, we identified eleven new phylogenetic clades, six of which were also morphologically characterized. Three of these novel clades were phylogenetically and morphologically similar to cigar-shaped type A1 cells, found in a wide range of surgeonfishes including Acanthurus nigrofuscus, while three were similar to smaller, rod-shaped type E that has not been phylogenetically classified thus far. Our results also confirmed that biogeography appears to have relatively little influence on Epulopiscium diversity, as clades found in the Great Barrier Reef and Hawaii were also recovered from the Red Sea. Although multiple symbiont clades inhabited a given species of host surgeonfish and multiple host species possessed a given symbiont clade, statistical analysis of host and symbiont phylogenies indicated significant cophylogeny, which in turn suggests co-evolutionary relationships. A cluster analysis of Epulopiscium sequences from previously published amplicon sequencing dataset revealed a similar pattern, where specific clades were consistently found in high abundance amongst closely related surgeonfishes. Differences in abundance may indicate specialization of clades to certain gut environments reflected by inferred differences in the host diets. Overall, our analysis identified a large phylogenetic diversity of Epulopiscium (up to 10% sequence divergence of 16S rRNA genes), which lets us hypothesize that there are multiple species that are spread across guts of different host species.
    • Hologenome analysis of two marine sponges with different microbiomes

      Ryu, Tae Woo; Seridi, Loqmane; Moitinho-Silva, Lucas; Oates, Matthew; Liew, Yi Jin; Mavromatis, Charalampos Harris; Wang, Xiaolei; Haywood, Annika; Lafi, Feras Fawzi; Kupresanin, Marija; Sougrat, Rachid; Alzahrani, Majed A.; Giles, Emily; Ghosheh, Yanal; Schunter, Celia Marei; Baumgarten, Sebastian; Berumen, Michael L.; Gao, Xin; Aranda, Manuel; Foret, Sylvain; Gough, Julian; Voolstra, Christian R.; Hentschel, Ute; Ravasi, Timothy (BMC Genomics, Springer Nature, 2016-02-29) [Article]
      Background Sponges (Porifera) harbor distinct microbial consortia within their mesohyl interior. We herein analysed the hologenomes of Stylissa carteri and Xestospongia testudinaria, which notably differ in their microbiome content. Results Our analysis revealed that S. carteri has an expanded repertoire of immunological domains, specifically Scavenger Receptor Cysteine-Rich (SRCR)-like domains, compared to X. testudinaria. On the microbial side, metatranscriptome analyses revealed an overrepresentation of potential symbiosis-related domains in X. testudinaria. Conclusions Our findings provide genomic insights into the molecular mechanisms underlying host-symbiont coevolution and may serve as a roadmap for future hologenome analyses.
    • Gene expression variation resolves species and individual strains among coral-associated dinoflagellates within the genus Symbiodinium

      Parkinson, John Everett; Baumgarten, Sebastian; Michell, Craig; Baums, Iliana B.; LaJeunesse, Todd C.; Voolstra, Christian R. (Genome Biology and Evolution, Oxford University Press (OUP), 2016-02-11) [Article]
      Reef-building corals depend on symbiotic mutualisms with photosynthetic dinoflagellates in the genus Symbiodinium. This large microalgal group comprises many highly divergent lineages (“Clades A-I”) and hundreds of undescribed species. Given their ecological importance, efforts have turned to genomic approaches to characterize the functional ecology of Symbiodinium. To date, investigators have only compared gene expression between representatives from separate clades—the equivalent of contrasting genera or families in other dinoflagellate groups—making it impossible to distinguish between clade-level and species-level functional differences. Here, we examined the transcriptomes of four species within one Symbiodinium clade (Clade B) at ~20,000 orthologous genes, as well as multiple isoclonal cell lines within species (i.e. cultured strains). These species span two major adaptive radiations within Clade B, each encompassing both host-specialized and ecologically cryptic taxa. Species-specific expression differences were consistently enriched for photosynthesis-related genes, likely reflecting selection pressures driving niche diversification. Transcriptional variation among strains involved fatty acid metabolism and biosynthesis pathways. Such differences among individuals are potentially a major source of physiological variation, contributing to the functional diversity of coral holobionts composed of unique host-symbiont genotype pairings. Our findings expand the genomic resources available for this important symbiont group and emphasize the power of comparative transcriptomics as a method for studying speciation processes and inter-individual variation in non-model organisms.
    • The role of marine reserves in the replenishment of a locally-impacted population of anemonefish on the Great Barrier Reef

      Bonin, Mary C.; Harrison, Hugo B.; Williamson, David H.; Frisch, Ashley J.; Saenz Agudelo, Pablo; Berumen, Michael L.; Jones, Geoffrey P. (Molecular Ecology, Wiley, 2016-01-19) [Article]
      The development of parentage analysis to track the dispersal of juvenile offspring has given us unprecedented insight into the population dynamics of coral reef fishes. These tools now have the potential to inform fisheries management and species conservation, particularly for small fragmented populations under threat from exploitation and disturbance. In this study we resolve patterns of larval dispersal for a population of the anemonefish Amphiprion melanopus in the Keppel Islands (southern Great Barrier Reef). Habitat loss and fishing appear to have impacted this population and a network of no-take marine reserves currently protects 75% of the potential breeders. Using parentage analysis, we estimate that 21% of recruitment in the island group was generated locally, and that breeding adults living in reserves were responsible for 79% (31 out of 39) of these of locally-produced juveniles. Overall, the network of reserves was fully connected via larval dispersal; however one reserve was identified as a critical source of larvae for the island group. The population in the Keppel Islands also appears to be well-connected to other source populations at least 60 km away, given that 79% (145 out of 184) of the juveniles sampled remained unassigned in the parentage analysis. We estimated the effective size of the A. melanopus metapopulation to be 745 (582-993 95% CI) and recommend continued monitoring of its genetic status. Maintaining connectivity with populations beyond the Keppel Islands and recovery of local recruitment habitat, potentially through active restoration of host anemone populations, will be important for its long-term persistence.