• Absence of genetic differentiation in the coral Pocillopora verrucosa along environmental gradients of the Saudi Arabian Red Sea

      Robitzch, Vanessa S.N.; Banguera Hinestroza, Eulalia; Sawall, Yvonne; Al-Sofyani, Abdulmohsin; Voolstra, Christian R. (Frontiers Media SA, 2015-02-11)
      The Red Sea is the world's northernmost tropical sea. The 2000 km long, but narrow basin creates distinct environmental conditions along its latitudinal spread. The Red Sea displays a pronounced salinity gradient from 41 to 37 PSU (north to south) with an opposing temperature gradient from 21 to 27°C in the north to 27–33.8°C in the south. The Red Sea further displays a decreasing nutrient gradient from south to north that can also influence underwater light fields due to higher phytoplankton content and turbidity. Despite this strong variation in temperature, salinity, nutrients, and light conditions, the Red Sea supports large and diverse coral reef ecosystems along its nearly entire coastline. Only few studies have targeted whether these prevailing gradients affect genetic connectivity of reef organisms in the Red Sea. In this study, we sampled the abundant reef-building coral Pocillopora verrucosa from 10 reefs along a latitudinal gradient in the Red Sea covering an area of more than 850 km. We used nine Pocillopora microsatellite markers to assess the underlying population genetic structure and effective population size. To assure the exclusion of cryptic species, all analyzed specimens were chosen from a single mitochondrial lineage. Despite large distances between sampled regions covering pronounced, but smooth temperature and salinity gradients, no significant genetic population structure was found. Rather, our data indicate panmixia and considerable gene flow among regions. The absence of population subdivision driven by environmental factors and over large geographic distances suggests efficient larval dispersal and successful settlement of recruits from a wide range of reef sites. It also advocates, broadcast spawning as the main reproductive strategy of Pocillopora verrucosa in the Red Sea as reflected by the absence of clones in sampled colonies. These factors might explain the success of Pocillopora species throughout the Indo-Pacific and Arabian Seas.
    • After continents divide: Comparative phylogeography of reef fishes from the Red Sea and Indian Ocean

      Dibattista, Joseph D.; Berumen, Michael L.; Gaither, Michelle R.; Rocha, Luiz A.; Eble, Jeff A.; Choat, John Howard; Craig, Matthew T.; Skillings, Derek J.; Bowen, Brian W. (Wiley, 2013-01-07)
      Aim: The Red Sea is a biodiversity hotspot characterized by a unique marine fauna and high endemism. This sea began forming c. 24 million years ago with the separation of the African and Arabian plates, and has been characterized by periods of desiccation, hypersalinity and intermittent connection to the Indian Ocean. We aim to evaluate the impact of these events on the genetic architecture of the Red Sea reef fish fauna. Location: Red Sea and Western Indian Ocean. Methods: We surveyed seven reef fish species from the Red Sea and adjacent Indian Ocean using mitochondrial DNA cytochrome c oxidase subunit I and cytochrome b sequences. To assess genetic variation and evolutionary connectivity within and between these regions, we estimated haplotype diversity (h) and nucleotide diversity (π), reconstructed phylogenetic relationships among haplotypes, and estimated gene flow and time of population separation using Bayesian coalescent-based methodology. Results: Our analyses revealed a range of scenarios from shallow population structure to diagnostic differences that indicate evolutionary partitions and possible cryptic species. Conventional molecular clocks and coalescence analyses indicated time-frames for divergence between these bodies of water ranging from 830,000 years to contemporary exchange or recent range expansion. Colonization routes were bidirectional, with some species moving from the Indian Ocean to the Red Sea compared with expansion out of the Red Sea for other species. Main conclusions: We conclude that: (1) at least some Red Sea reef fauna survived multiple salinity crises; (2) endemism is higher in the Red Sea than previously reported; and (3) the Red Sea is an evolutionary incubator, occasionally contributing species to the adjacent Indian Ocean. The latter two conclusions - elevated endemism and species export - indicate a need for enhanced conservation priorities for the Red Sea. © 2013 Blackwell Publishing Ltd.
    • 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 (Springer Nature, 2016-09-01)
      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.
    • 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, 2016-04-05)
      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.
    • Assessing Symbiodinium diversity in scleractinian corals via next-generation sequencing-based genotyping of the ITS2 rDNA region

      Arif, Chatchanit; Daniels, Camille; Bayer, Till; Banguera Hinestroza, Eulalia; Barbrook, Adrian; Howe, Christopher J.; LaJeunesse, Todd C.; Voolstra, Christian R. (Wiley-Blackwell, 2014-09)
      The persistence of coral reef ecosystems relies on the symbiotic relationship between scleractinian corals and intracellular, photosynthetic dinoflagellates in the genus Symbiodinium. Genetic evidence indicates that these symbionts are biologically diverse and exhibit discrete patterns of environmental and host distribution. This makes the assessment of Symbiodinium diversity critical to understanding the symbiosis ecology of corals. Here, we applied pyrosequencing to the elucidation of Symbiodinium diversity via analysis of the internal transcribed spacer 2 (ITS2) region, a multicopy genetic marker commonly used to analyse Symbiodinium diversity. Replicated data generated from isoclonal Symbiodinium cultures showed that all genomes contained numerous, yet mostly rare, ITS2 sequence variants. Pyrosequencing data were consistent with more traditional denaturing gradient gel electrophoresis (DGGE) approaches to the screening of ITS2 PCR amplifications, where the most common sequences appeared as the most intense bands. Further, we developed an operational taxonomic unit (OTU)-based pipeline for Symbiodinium ITS2 diversity typing to provisionally resolve ecologically discrete entities from intragenomic variation. A genetic distance cut-off of 0.03 collapsed intragenomic ITS2 variants of isoclonal cultures into single OTUs. When applied to the analysis of field-collected coral samples, our analyses confirm that much of the commonly observed Symbiodinium ITS2 diversity can be attributed to intragenomic variation. We conclude that by analysing Symbiodinium populations in an OTU-based framework, we can improve objectivity, comparability and simplicity when assessing ITS2 diversity in field-based studies.
    • Assessment of Zooplankton Community Composition along a Depth Profile in the Central Red Sea

      Pearman, John K.; Irigoien, Xabier (Public Library of Science (PLoS), 2015-07-17)
      The composition of zooplankton in the water column has received limited attention in the main body of the Red Sea and this study investigates the change in the community both spatially and temporally across 11 stations in the central Red Sea. Using molecular methods to target the v9 region of the 18S rRNA gene a total of approximately 11.5 million reads were sequenced resulting in 2528 operational taxonomic units (OTUs) at 97% similarity. The phylum Arthropoda dominated in terms of reads accounting for on average 86.2% and 65.3% for neuston nets and vertical multinets respectively. A reduction in the number of OTUs was noticed with depth for both total metazoa and Maxillopoda whilst there was also a significant change in the composition of the Maxillopoda community. The genus Corycaeus had a higher proportion of reads in the epipelagic zone with Pleuromamma becoming increasingly dominant with depth. No significant difference was observed in the community between night and day sampling however there was a significant difference in the zooplankton community between two sampling periods separated by 10 days.
    • Association of coral algal symbionts with a diverse viral community responsive to heat shock

      Brüwer, Jan D.; Agrawal, Shobhit; Liew, Yi Jin; Aranda, Manuel; Voolstra, Christian R. (Springer Nature, 2017-08-17)
      Stony corals provide the structural foundation of coral reef ecosystems and are termed holobionts given they engage in symbioses, in particular with photosynthetic dinoflagellates of the genus Symbiodinium. Besides Symbiodinium, corals also engage with bacteria affecting metabolism, immunity, and resilience of the coral holobiont, but the role of associated viruses is largely unknown. In this regard, the increase of studies using RNA sequencing (RNA-Seq) to assess gene expression provides an opportunity to elucidate viral signatures encompassed within the data via careful delineation of sequence reads and their source of origin.Here, we re-analyzed an RNA-Seq dataset from a cultured coral symbiont (Symbiodinium microadriaticum, Clade A1) across four experimental treatments (control, cold shock, heat shock, dark shock) to characterize associated viral diversity, abundance, and gene expression. Our approach comprised the filtering and removal of host sequence reads, subsequent phylogenetic assignment of sequence reads of putative viral origin, and the assembly and analysis of differentially expressed viral genes. About 15.46% (123 million) of all sequence reads were non-host-related, of which <1% could be classified as archaea, bacteria, or virus. Of these, 18.78% were annotated as virus and comprised a diverse community consistent across experimental treatments. Further, non-host related sequence reads assembled into 56,064 contigs, including 4856 contigs of putative viral origin that featured 43 differentially expressed genes during heat shock. The differentially expressed genes included viral kinases, ubiquitin, and ankyrin repeat proteins (amongst others), which are suggested to help the virus proliferate and inhibit the algal host's antiviral response.Our results suggest that a diverse viral community is associated with coral algal endosymbionts of the genus Symbiodinium, which prompts further research on their ecological role in coral health and resilience.
    • Bacterial community dynamics are linked to patterns of coral heat tolerance

      Ziegler, Maren; Seneca, Francois O.; Yum, Lauren; Palumbi, Stephen R.; Voolstra, Christian R. (Springer Nature, 2017-02-10)
      Ocean warming threatens corals and the coral reef ecosystem. Nevertheless, corals can be adapted to their thermal environment and inherit heat tolerance across generations. In addition, the diverse microbes that associate with corals have the capacity for more rapid change, potentially aiding the adaptation of long-lived corals. Here, we show that the microbiome of reef corals is different across thermally variable habitats and changes over time when corals are reciprocally transplanted. Exposing these corals to thermal bleaching conditions changes the microbiome for heat-sensitive corals, but not for heat-tolerant corals growing in habitats with natural high heat extremes. Importantly, particular bacterial taxa predict the coral host response in a short-term heat stress experiment. Such associations could result from parallel responses of the coral and the microbial community to living at high natural temperatures. A competing hypothesis is that the microbial community and coral heat tolerance are causally linked.
    • Bacterial diversity in the bottom boundary layer of the inner continental shelf of Oregon, USA

      Bertagnolli, AD; Treusch, AH; Mason, OU; Stingl, Ulrich; Vergin, KL; Chan, F; Beszteri, B; Giovannoni, SJ (Inter-Research Science Center, 2011-6-21)
      There have been few studies of the bacterial community within the bottom boundary layer (BBL) the turbulent region of the water column above the benthos in shallow seas. Typically, the BBL has large amounts of particulate organic matter suspended by turbulence, and it is often the first region of the water column to become hypoxic when oxygen declines. Communities at the surface (5 m) and in the BBL (1 to 10 m above the sea floor) were compared by terminal restriction fragment length polymorphism (T-RFLP) analysis and sequencing of the 16S rRNA gene. Multivariate statistical methods (hierarchical clustering, non-metric multidimensional scaling, and analysis of similarity (ANOSIM)) indicated that the microbial community of the BBL is distinct from the surface community. ANOSIM supported the distinction between surface and BBLs (R values 0.427 and 0.463, based on analysis with restriction enzymes BsuR1 and Hin6I, respectively, p < 0.1%). Six terminal restriction fragments showed an increase in abundance with depth. Cloning, screening and sequencing identified these as a novel environmental clade (Eastern North Pacific Chromatiales (ENPC) clade), the ARTIC96BD-19 clade of Gammaproteobacteria, the 6N14 and Agg8 clades of the phylum Planctomycetes, the OM60/NOR5 clade of Gammaproteobacteria, and uncultivated members of the Roseobacter clade in the MB11C09 and ULA23 subgroups. To the best of our knowledge, this analysis is the first to focus on the unique composition of microbial communities of the BBL in shallow, inner-shelf regions off the coast of Oregon, USA, and the first to report that an uncharacterized clade of Chromatiales is indigenous in this habitat.
    • Bacterial profiling of White Plague Disease across corals and oceans indicates a conserved and distinct disease microbiome

      Roder, C.; Arif, C.; Daniels, C.; Weil, E.; Voolstra, Christian R. (Wiley-Blackwell, 2014-01-29)
      Coral diseases are characterized by microbial community shifts in coral mucus and tissue, but causes and consequences of these changes are vaguely understood due to the complexity and dynamics of coral-associated bacteria. We used 16S rRNA gene microarrays to assay differences in bacterial assemblages of healthy and diseased colonies displaying White Plague Disease (WPD) signs from two closely related Caribbean coral species, Orbicella faveolata and Orbicella franksi. Analysis of differentially abundant operational taxonomic units (OTUs) revealed strong differences between healthy and diseased specimens, but not between coral species. A subsequent comparison to data from two Indo-Pacific coral species (Pavona duerdeni and Porites lutea) revealed distinct microbial community patterns associated with ocean basin, coral species and health state. Coral species were clearly separated by site, but also, the relatedness of the underlying bacterial community structures resembled the phylogenetic relationship of the coral hosts. In diseased samples, bacterial richness increased and putatively opportunistic bacteria were consistently more abundant highlighting the role of opportunistic conditions in structuring microbial community patterns during disease. Our comparative analysis shows that it is possible to derive conserved bacterial footprints of diseased coral holobionts that might help in identifying key bacterial species related to the underlying etiopathology. Furthermore, our data demonstrate that similar-appearing disease phenotypes produce microbial community patterns that are consistent over coral species and oceans, irrespective of the putative underlying pathogen. Consequently, profiling coral diseases by microbial community structure over multiple coral species might allow the development of a comparative disease framework that can inform on cause and relatedness of coral diseases. 2013 The Authors Molecular Ecology John Wiley & Sons Ltd.
    • Bacterial profiling of White Plague Disease in a comparative coral species framework.

      Roder, Cornelia; Arif, Chatchanit; Bayer, Till; Aranda, Manuel; Daniels, Camille Arian; Shibl, Ahmed A.; Chavanich, Suchana; Voolstra, Christian R. (Springer Nature, 2014-01)
      Coral reefs are threatened throughout the world. A major factor contributing to their decline is outbreaks and propagation of coral diseases. Due to the complexity of coral-associated microbe communities, little is understood in terms of disease agents, hosts and vectors. It is known that compromised health in corals is correlated with shifts in bacterial assemblages colonizing coral mucus and tissue. However, general disease patterns remain, to a large extent, ambiguous as comparative studies over species, regions, or diseases are scarce. Here, we compare bacterial assemblages of samples from healthy (HH) colonies and such displaying signs of White Plague Disease (WPD) of two different coral species (Pavona duerdeni and Porites lutea) from the same reef in Koh Tao, Thailand, using 16S rRNA gene microarrays. In line with other studies, we found an increase of bacterial diversity in diseased (DD) corals, and a higher abundance of taxa from the families that include known coral pathogens (Alteromonadaceae, Rhodobacteraceae, Vibrionaceae). In our comparative framework analysis, we found differences in microbial assemblages between coral species and coral health states. Notably, patterns of bacterial community structures from HH and DD corals were maintained over species boundaries. Moreover, microbes that differentiated the two coral species did not overlap with microbes that were indicative of HH and DD corals. This suggests that while corals harbor distinct species-specific microbial assemblages, disease-specific bacterial abundance patterns exist that are maintained over coral species boundaries.
    • Bicarbonate transporters in corals point towards a key step in the evolution of cnidarian calcification

      Zoccola, Didier; Ganot, Philippe; Bertucci, Anthony; Caminiti-Segonds, Natacha; Techer, Nathalie; Voolstra, Christian R.; Aranda, Manuel; Tambutté, Eric; Allemand, Denis; Casey, Joseph R; Tambutté, Sylvie (Nature Publishing Group, 2015-06-04)
      The bicarbonate ion (HCO3−) is involved in two major physiological processes in corals, biomineralization and photosynthesis, yet no molecular data on bicarbonate transporters are available. Here, we characterized plasma membrane-type HCO3− transporters in the scleractinian coral Stylophora pistillata. Eight solute carrier (SLC) genes were found in the genome: five homologs of mammalian-type SLC4 family members, and three of mammalian-type SLC26 family members. Using relative expression analysis and immunostaining, we analyzed the cellular distribution of these transporters and conducted phylogenetic analyses to determine the extent of conservation among cnidarian model organisms. Our data suggest that the SLC4γ isoform is specific to scleractinian corals and responsible for supplying HCO3− to the site of calcification. Taken together, SLC4γ appears to be one of the key genes for skeleton building in corals, which bears profound implications for our understanding of coral biomineralization and the evolution of scleractinian corals within cnidarians.
    • Biogeography and molecular diversity of coral symbionts in the genus Symbiodinium around the Arabian Peninsula

      Ziegler, Maren; Arif, Chatchanit; Burt, John A.; Dobretsov, Sergey; Roder, Cornelia; Lajeunesse, Todd C.; Voolstra, Christian R. (Wiley-Blackwell, 2017-01-02)
      Aim: Coral reefs rely on the symbiosis between scleractinian corals and intracellular, photosynthetic dinoflagellates of the genus Symbiodinium making the assessment of symbiont diversity critical to our understanding of ecological resilience of these ecosystems. This study characterizes Symbiodinium diversity around the Arabian Peninsula, which contains some of the most thermally diverse and understudied reefs on Earth. Location: Shallow water coral reefs throughout the Red Sea (RS), Sea of Oman (SO), and Persian/Arabian Gulf (PAG). Methods: Next-generation sequencing of the ITS2 marker gene was used to assess Symbiodinium community composition and diversity comprising 892 samples from 46 hard and soft coral genera. Results: Corals were associated with a large diversity of Symbiodinium, which usually consisted of one or two prevalent symbiont types and many types at low abundance. Symbiodinium communities were strongly structured according to geographical region and to a lesser extent by coral host identity. Overall symbiont communities were composed primarily of species from clade A and C in the RS, clade A, C, and D in the SO, and clade C and D in the PAG, representing a gradual shift from C- to D-dominated coral hosts. The analysis of symbiont diversity in an Operational Taxonomic Unit (OTU)-based framework allowed the identification of differences in symbiont taxon richness over geographical regions and host genera. Main conclusions: Our study represents a comprehensive overview over biogeography and molecular diversity of Symbiodinium in the Arabian Seas, where coral reefs thrive in one of the most extreme environmental settings on the planet. As such our data will serve as a baseline for further exploration into the effects of environmental change on host-symbiont pairings and the identification and ecological significance of Symbiodinium types from regions already experiencing 'Future Ocean' conditions.
    • Biosynthetic multitasking facilitates thalassospiramide structural diversity in marine bacteria

      Ross, Avena C.; Xü, Ying; Lu, Liang; Kersten, Roland D.; Shao, Zongze; Al-Suwailem, Abdulaziz M.; Dorrestein, Pieter C.; Qian, Peiyuan; Moore, Bradley S. (American Chemical Society, 2013-01-23)
      Thalassospiramides A and B are immunosuppressant cyclic lipopeptides first reported from the marine α-proteobacterium Thalassospira sp. CNJ-328. We describe here the discovery and characterization of an extended family of 14 new analogues from four Tistrella and Thalassospira isolates. These potent calpain 1 protease inhibitors belong to six structure classes in which the length and composition of the acylpeptide side chain varies extensively. Genomic sequence analysis of the thalassospiramide-producing microbes revealed related, genus-specific biosynthetic loci encoding hybrid nonribosomal peptide synthetase/polyketide synthases consistent with thalassospiramide assembly. The bioinformatics analysis of the gene clusters suggests that structural diversity, which ranges from the 803.4 Da thalassospiramide C to the 1291.7 Da thalassospiramide F, results from a complex sequence of reactions involving amino acid substrate channeling and enzymatic multimodule skipping and iteration. Preliminary biochemical analysis of the N-terminal nonribosomal peptide synthetase module from the Thalassospira TtcA megasynthase supports a biosynthetic model in which in cis amino acid activation competes with in trans activation to increase the range of amino acid substrates incorporated at the N terminus. © 2012 American Chemical Society.
    • Blind to morphology: Genetics identifies several widespread ecologically common species and few endemics among Indo-Pacific cauliflower corals (Pocillopora, Scleractinia)

      Pinzón, Jorge H C; Sampayo, Eugenia M.; Cox, Evelyn F.; Chauka, Leonard J.; Chen, Chaolun Allen; Voolstra, Christian R.; LaJeunesse, Todd C. (Wiley, 2013-04-05)
      Aim: Using high-resolution genetic markers on samples gathered from across their wide distributional range, we endeavoured to delimit species diversity in reef-building Pocillopora corals. They are common, ecologically important, and widespread throughout the Indo-Pacific, but their phenotypic plasticity in response to environmental conditions and their nearly featureless microskeletal structures confound taxonomic assignments and limit an understanding of their ecology and evolution. Location: Indo-Pacific, Red Sea, Arabian/Persian Gulf. Methods: Sequence analysis of nuclear ribosomal (internal transcribed spacer 2, ITS2) and mitochondrial (open reading frame) loci were combined with population genetic data (seven microsatellite loci) for Pocillopora samples collected throughout the Indo-Pacific, Red Sea and Arabian Gulf, in order to assess the evolutionary divergence, reproductive isolation, frequency of hybridization and geographical distributions of the genus. Results: Between five and eight genetically distinct lineages comparable to species were identified with minimal or no hybridization between them. Colony morphology was generally incongruent with genetics across the full range of sampling, and the total number of species is apparently consistent with lower estimates from competing morphologically based hypotheses (about seven or eight taxa). The most commonly occurring genetic lineages were widely distributed and exhibited high dispersal and gene flow, factors that have probably minimized allopatric speciation. Uniquely among scleractinian genera, this genus contains a monophyletic group of broadcast spawners that evolved recently from an ancestral brooder. Main conclusions: The delineation of species diversity guided by genetics fundamentally advances our understanding of Pocillopora geographical distributions, ecology and evolution. Because traditional diagnostic features of colony and branch morphology are proving to be of limited utility, the identification of Pocillopora species for future ecological and experimental work should rely on genetic characters that will improve research and aid in conservation strategies for these and other reef-building corals, including the detection of real and mistaken endemic populations. © 2013 Blackwell Publishing Ltd.
    • Carotenoid metabolic profiling and transcriptome-genome mining reveal functional equivalence among blue-pigmented copepods and appendicularia

      Mojib, Nazia; Amad, Maan H.; Thimma, Manjula; Aldanondo, Naroa; Kumaran, Mande; Irigoien, Xabier (Wiley-Blackwell, 2014-06)
      The tropical oligotrophic oceanic areas are characterized by high water transparency and annual solar radiation. Under these conditions, a large number of phylogenetically diverse mesozooplankton species living in the surface waters (neuston) are found to be blue pigmented. In the present study, we focused on understanding the metabolic and genetic basis of the observed blue phenotype functional equivalence between the blue-pigmented organisms from the phylum Arthropoda, subclass Copepoda (Acartia fossae) and the phylum Chordata, class Appendicularia (Oikopleura dioica) in the Red Sea. Previous studies have shown that carotenoid–protein complexes are responsible for blue coloration in crustaceans. Therefore, we performed carotenoid metabolic profiling using both targeted and nontargeted (high-resolution mass spectrometry) approaches in four different blue-pigmented genera of copepods and one blue-pigmented species of appendicularia. Astaxanthin was found to be the principal carotenoid in all the species. The pathway analysis showed that all the species can synthesize astaxanthin from β-carotene, ingested from dietary sources, via 3-hydroxyechinenone, canthaxanthin, zeaxanthin, adonirubin or adonixanthin. Further, using de novo assembled transcriptome of blue A. fossae (subclass Copepoda), we identified highly expressed homologous β-carotene hydroxylase enzymes and putative carotenoid-binding proteins responsible for astaxanthin formation and the blue phenotype. In blue O. dioica (class Appendicularia), corresponding putative genes were identified from the reference genome. Collectively, our data provide molecular evidences for the bioconversion and accumulation of blue astaxanthin–protein complexes underpinning the observed ecological functional equivalence and adaptive convergence among neustonic mesozooplankton.
    • A catalogue of 136 microbial draft genomes from Red Sea metagenomes

      Haroon, Mohamed; Thompson, Luke R.; Parks, Donovan H.; Hugenholtz, Philip; Stingl, Ulrich (Springer Nature, 2016-07-05)
      Earth is expected to continue warming and the Red Sea is a model environment for understanding the effects of global warming on ocean microbiomes due to its unusually high temperature, salinity and solar irradiance. However, most microbial diversity analyses of the Red Sea have been limited to cultured representatives and single marker gene analyses, hence neglecting the substantial uncultured majority. Here, we report 136 microbial genomes (completion minus contamination is ≥50%) assembled from 45 metagenomes from eight stations spanning the Red Sea and taken from multiple depths between 10 to 500 m. Phylogenomic analysis showed that most of the retrieved genomes belong to seven different phyla of known marine microbes, but more than half representing currently uncultured species. The open-access data presented here is the largest number of Red Sea representative microbial genomes reported in a single study and will help facilitate future studies in understanding the physiology of these microorganisms and how they have adapted to the relatively harsh conditions of the Red Sea.
    • Characterization of new microsatellite loci for population genetic studies in the Smooth Cauliflower Coral (Stylophora sp.)

      Banguera-Hinestroza, E.; Saenz-Agudelo, P.; Bayer, T.; Berumen, Michael L.; Voolstra, Christian R. (Springer Nature, 2013-01-09)
      A total of one hundred microsatellites loci were selected from the draft genome of Stylophora pistillata and evaluated in previously characterized samples of Stylophora cf pistillata from the Red Sea. 17 loci were amplified successfully and tested in 24 individuals from samples belonging to a single population from the central region of the Red Sea. The number of alleles ranged from 3 to 15 alleles per locus, while observed heterozygosity ranged from 0. 292 to 0. 95. Six of these loci showed significant deviations from Hardy-Weinberg equilibrium (HWE) expectations, and 4/136 paired loci comparisons suggested linkage disequilibrium after Bonferroni corrections. After excluding loci with significant HWE deviation and evidence of null alleles, average genetic diversity over loci in the population studied (N = 24, Nloci = 11) was 0. 701 ± 0. 380. This indicates that these loci can be used effectively to evaluate genetic diversity and undertake population genetics studies in Stylophora sp. populations. 2013 The Author(s).
    • The chloroplast genome of a symbiodinium sp. clade C3 isolate

      Barbrook, Adrian C.; Voolstra, Christian R.; Howe, Christopher J. (Elsevier BV, 2014-01)
      Dinoflagellate algae of the genus Symbiodinium form important symbioses within corals and other benthic marine animals. Dinoflagellates possess an extremely reduced plastid genome relative to those examined in plants and other algae. In dinoflagellates the plastid genes are located on small plasmids, commonly referred to as 'minicircles'. However, the chloroplast genomes of dinoflagellates have only been extensively characterised from a handful of species. There is also evidence of considerable variation in the chloroplast genome organisation across those species that have been examined. We therefore characterised the chloroplast genome from an environmental coral isolate, in this case containing a symbiont belonging to the Symbiodinium sp. clade C3. The gene content of the genome is well conserved with respect to previously characterised genomes. However, unlike previously characterised dinoflagellate chloroplast genomes we did not identify any 'empty' minicircles. The sequences of this chloroplast genome show a high rate of evolution relative to other algal species. Particularly notable was a surprisingly high level of sequence divergence within the core polypeptides of photosystem I, the reasons for which are currently unknown. This chloroplast genome also possesses distinctive codon usage and GC content. These features suggest that chloroplast genomes in Symbiodinium are highly plastic. © 2013 Adrian C. Barbrook.
    • Combined analyses of the ITS loci and the corresponding 16S rRNA genes reveal high micro- and macrodiversity of SAR11 populations in the Red Sea.

      Ngugi, David; Stingl, Ulrich (Public Library of Science (PLoS), 2012-11-20)
      Bacteria belonging to the SAR11 clade are among the most abundant prokaryotes in the pelagic zone of the ocean. 16S rRNA gene-based analyses indicate that they constitute up to 60% of the bacterioplankton community in the surface waters of the Red Sea. This extremely oligotrophic water body is further characterized by an epipelagic zone, which has a temperature above 24 °C throughout the year, and a remarkable uniform temperature (~22 °C) and salinity (~41 psu) from the mixed layer (~200 m) to the bottom at over 2000 m depth. Despite these conditions that set it apart from other marine environments, the microbiology of this ecosystem is still vastly understudied. Prompted by the limited phylogenetic resolution of the 16S rRNA gene, we extended our previous study by sequencing the internal transcribed spacer (ITS) region of SAR11 in different depths of the Red Sea's water column together with the respective 16S fragment. The overall diversity captured by the ITS loci was ten times higher than that of the corresponding 16S rRNA genes. Moreover, species estimates based on the ITS showed a highly diverse population of SAR11 in the mixed layer that became diminished in deep isothermal waters, which was in contrast to results of the related 16S rRNA genes. While the 16S rRNA gene-based sequences clustered into three phylogenetic subgroups, the related ITS fragments fell into several phylotypes that showed clear depth-dependent shifts in relative abundances. Blast-based analyses not only documented the observed vertical partitioning and universal co-occurrence of specific phylotypes in five other distinct oceanic provinces, but also highlighted the influence of ecosystem-specific traits (e.g., temperature, nutrient availability, and concentration of dissolved oxygen) on the population dynamics of this ubiquitous marine bacterium.