Recent Submissions

  • First insight into the viral community of the cnidarian model metaorganism Aiptasia using RNA-Seq data

    Brüwer, Jan D.; Voolstra, Christian R. (PeerJ, PeerJ, 2018-03-01) [Article]
    Current research posits that all multicellular organisms live in symbioses with associated microorganisms and form so-called metaorganisms or holobionts. Cnidarian metaorganisms are of specific interest given that stony corals provide the foundation of the globally threatened coral reef ecosystems. To gain first insight into viruses associated with the coral model system Aiptasia (sensu Exaiptasia pallida), we analyzed an existing RNA-Seq dataset of aposymbiotic, partially populated, and fully symbiotic Aiptasia CC7 anemones with Symbiodinium. Our approach included the selective removal of anemone host and algal endosymbiont sequences and subsequent microbial sequence annotation. Of a total of 297 million raw sequence reads, 8.6 million (∼3%) remained after host and endosymbiont sequence removal. Of these, 3,293 sequences could be assigned as of viral origin. Taxonomic annotation of these sequences suggests that Aiptasia is associated with a diverse viral community, comprising 116 viral taxa covering 40 families. The viral assemblage was dominated by viruses from the families Herpesviridae (12.00%), Partitiviridae (9.93%), and Picornaviridae (9.87%). Despite an overall stable viral assemblage, we found that some viral taxa exhibited significant changes in their relative abundance when Aiptasia engaged in a symbiotic relationship with Symbiodinium. Elucidation of viral taxa consistently present across all conditions revealed a core virome of 15 viral taxa from 11 viral families, encompassing many viruses previously reported as members of coral viromes. Despite the non-random selection of viral genetic material due to the nature of the sequencing data analyzed, our study provides a first insight into the viral community associated with Aiptasia. Similarities of the Aiptasia viral community with those of corals corroborate the application of Aiptasia as a model system to study coral holobionts. Further, the change in abundance of certain viral taxa across different symbiotic states suggests a role of viruses in the algal endosymbiosis, but the functional significance of this remains to be determined.
  • Using ezRAD to reconstruct the complete mitochondrial genome of Porites fontanesii (Cnidaria: Scleractinia)

    Terraneo, Tullia Isotta; Arrigoni, Roberto; Benzoni, Francesca; Forsman, Zac H.; Berumen, Michael L. (Mitochondrial DNA Part B, Informa UK Limited, 2018-02-09) [Article]
    Corals in the genus Porites are among the major framework builders of reef structures worldwide, yet the genus has been challenging to study due to a lack of informative molecular markers. Here, we used ezRAD sequencing to reconstruct the complete mitochondrial genome of Porites fontanesii (GenBank accession number MG754069), a widespread coral species endemic to the Red Sea and Gulf of Aden. The gene arrangement of P. fontanesii did not differ from other Scleractinia and consisted of 18,658 bp, organized in 13 protein-coding genes, 2 rRNA genes, and 2 tRNA genes. This mitochondrial genome contributes essential data to work towards a better understanding of evolutionary relationships within Porites.
  • Dominance of Endozoicomonas bacteria throughout coral bleaching and mortality suggests structural inflexibility of the Pocillopora verrucosa microbiome

    Pogoreutz, Claudia; Radecker, Nils; Cardenas, Anny; Gärdes, Astrid; Wild, Christian; Voolstra, Christian R. (Ecology and Evolution, Wiley, 2018-01-25) [Article]
    The importance of Symbiodinium algal endosymbionts and a diverse suite of bacteria for coral holobiont health and functioning are widely acknowledged. Yet, we know surprisingly little about microbial community dynamics and the stability of host-microbe associations under adverse environmental conditions. To gain insight into the stability of coral host-microbe associations and holobiont structure, we assessed changes in the community structure of Symbiodinium and bacteria associated with the coral Pocillopora verrucosa under excess organic nutrient conditions. Pocillopora-associated microbial communities were monitored over 14 days in two independent experiments. We assessed the effect of excess dissolved organic nitrogen (DON) and excess dissolved organic carbon (DOC). Exposure to excess nutrients rapidly affected coral health, resulting in two distinct stress phenotypes: coral bleaching under excess DOC and severe tissue sloughing (>90% tissue loss resulting in host mortality) under excess DON. These phenotypes were accompanied by structural changes in the Symbiodinium community. In contrast, the associated bacterial community remained remarkably stable and was dominated by two Endozoicomonas phylotypes, comprising on average 90% of 16S rRNA gene sequences. This dominance of Endozoicomonas even under conditions of coral bleaching and mortality suggests the bacterial community of P. verrucosa may be rather inflexible and thereby unable to respond or acclimatize to rapid changes in the environment, contrary to what was previously observed in other corals. In this light, our results suggest that coral holobionts might occupy structural landscapes ranging from a highly flexible to a rather inflexible composition with consequences for their ability to respond to environmental change.
  • Large-scale ocean connectivity and planktonic body size

    Villarino, Ernesto; Watson, James R.; Jönsson, Bror; Gasol, Josep M.; Salazar, Guillem; Acinas, Silvia G.; Estrada, Marta; Massana, Ramón; Logares, Ramiro; Giner, Caterina R.; Pernice, Massimo C.; Olivar, M. Pilar; Citores, Leire; Corell, Jon; Rodríguez-Ezpeleta, Naiara; Acuña, José Luis; Molina-Ramírez, Axayacatl; González-Gordillo, J. Ignacio; Cózar, Andrés; Martí, Elisa; Cuesta, José A.; Agusti, Susana; Fraile-Nuez, Eugenio; Duarte, Carlos M.; Irigoien, Xabier; Chust, Guillem (Nature Communications, Springer Nature, 2018-01-10) [Article]
    Global patterns of planktonic diversity are mainly determined by the dispersal of propagules with ocean currents. However, the role that abundance and body size play in determining spatial patterns of diversity remains unclear. Here we analyse spatial community structure - β-diversity - for several planktonic and nektonic organisms from prokaryotes to small mesopelagic fishes collected during the Malaspina 2010 Expedition. β-diversity was compared to surface ocean transit times derived from a global circulation model, revealing a significant negative relationship that is stronger than environmental differences. Estimated dispersal scales for different groups show a negative correlation with body size, where less abundant large-bodied communities have significantly shorter dispersal scales and larger species spatial turnover rates than more abundant small-bodied plankton. Our results confirm that the dispersal scale of planktonic and micro-nektonic organisms is determined by local abundance, which scales with body size, ultimately setting global spatial patterns of diversity.
  • Evidence for miRNA-mediated modulation of the host transcriptome in cnidarian-dinoflagellate symbiosis

    Baumgarten, Sebastian; Cziesielski, Maha Joana; Thomas, Ludivine; Michell, Craig; Esherick, Lisl Y.; Pringle, John R.; Aranda, Manuel; Voolstra, Christian R. (Molecular Ecology, Wiley, 2017-12-23) [Article]
    Reef-building corals and other cnidarians living in symbiotic relationships with intracellular, photosynthetic dinoflagellates in the genus Symbiodinium undergo transcriptomic changes during infection with the algae and maintenance of the endosymbiont population. However, the precise regulatory mechanisms modulating the host transcriptome are unknown. Here we report apparent post-transcriptional gene regulation by miRNAs in the sea anemone Aiptasia, a model system for cnidarian-dinoflagellate endosymbiosis. Aiptasia encodes mainly species-specific miRNAs, and there appears to have been recent differentiation within the Aiptasia genome of miRNAs that are commonly conserved among anthozoan cnidarians. Analysis of miRNA expression showed that both conserved and species-specific miRNAs are differentially expressed in response to endosymbiont infection. Using cross-linking immunoprecipitation of Argonaute, the central protein of the miRNA-induced silencing complex, we identified miRNA binding sites on a transcriptome-wide scale and found that the targets of the miRNAs regulated in response to symbiosis include genes previously implicated in biological processes related to Symbiodinium infection. Our study shows that cnidarian miRNAs recognize their mRNA targets via high-complementarity target binding and suggests that miRNA-mediated modulations of genes and pathways are important during the onset and maintenance of cnidarian-dinoflagellate endosymbiosis. This article is protected by copyright. All rights reserved.
  • Comparative analysis of the genomes of Stylophora pistillata and Acropora digitifera provides evidence for extensive differences between species of corals

    Voolstra, Christian R.; Li, Yong; Liew, Yi Jin; Baumgarten, Sebastian; Zoccola, Didier; Flot, Jean-François; Tambutté, Sylvie; Allemand, Denis; Aranda, Manuel (Scientific Reports, Springer Nature, 2017-12-08) [Article]
    Stony corals form the foundation of coral reef ecosystems. Their phylogeny is characterized by a deep evolutionary divergence that separates corals into a robust and complex clade dating back to at least 245 mya. However, the genomic consequences and clade-specific evolution remain unexplored. In this study we have produced the genome of a robust coral, Stylophora pistillata, and compared it to the available genome of a complex coral, Acropora digitifera. We conducted a fine-scale gene-based analysis focusing on ortholog groups. Among the core set of conserved proteins, we found an emphasis on processes related to the cnidarian-dinoflagellate symbiosis. Genes associated with the algal symbiosis were also independently expanded in both species, but both corals diverged on the identity of ortholog groups expanded, and we found uneven expansions in genes associated with innate immunity and stress response. Our analyses demonstrate that coral genomes can be surprisingly disparate. Future analyses incorporating more genomic data should be able to determine whether the patterns elucidated here are not only characteristic of the differences between S. pistillata and A. digitifera but also representative of corals from the robust and complex clade at large.
  • Rare symbionts may contribute to the resilience of coral–algal assemblages

    Ziegler, Maren; Eguíluz, Víctor M; Duarte, Carlos M.; Voolstra, Christian R. (The ISME Journal, Springer Nature, 2017-12-01) [Article]
    The association between corals and photosynthetic dinoflagellates (Symbiodinium spp.) is the key to the success of reef ecosystems in highly oligotrophic environments, but it is also their Achilles‘ heel due to its vulnerability to local stressors and the effects of climate change. Research during the last two decades has shaped a view that coral host–Symbiodinium pairings are diverse, but largely exclusive. Deep sequencing has now revealed the existence of a rare diversity of cryptic Symbiodinium assemblages within the coral holobiont, in addition to one or a few abundant algal members. While the contribution of the most abundant resident Symbiodinium species to coral physiology is widely recognized, the significance of the rare and low abundant background Symbiodinium remains a matter of debate. In this study, we assessed how coral–Symbiodinium communities assemble and how rare and abundant components together constitute the Symbiodinium community by analyzing 892 coral samples comprising >110 000 unique Symbiodinium ITS2 marker gene sequences. Using network modeling, we show that host–Symbiodinium communities assemble in non-random ‘clusters‘ of abundant and rare symbionts. Symbiodinium community structure follows the same principles as bacterial communities, for which the functional significance of rare members (the ‘rare bacterial biosphere’) has long been recognized. Importantly, the inclusion of rare Symbiodinium taxa in robustness analyses revealed a significant contribution to the stability of the host–symbiont community overall. As such, it highlights the potential functions rare symbionts may provide to environmental resilience of the coral holobiont.
  • Neurobiology of pair bonding in fishes; convergence of neural mechanisms across distant vertebrate lineages

    Nowicki, Jessica; Pratchett, Morgan; Walker, Stefan; Coker, Darren James; O'Connell, Lauren A. (Cold Spring Harbor Laboratory, 2017-11-14) [Preprint]
    Pair bonding has independently evolved numerous times among vertebrates. The governing neural mechanisms of pair bonding have only been studied in depth in the mammalian model species, the prairie vole, Microtus ochrogaster. In this species, oxytocin (OT), arginine vasopressin (AVP), dopamine (DA), and opioid (OP) systems play key roles in signaling in the formation and maintenance of pair bonding by targeting specific social and reward-mediating brain regions. By contrast, the neural basis of pair bonding is poorly studied in other vertebrates, and especially those of early origins, limiting our understanding of the evolutionary history of pair bonding regulatory mechanisms. We compared receptor gene expression between pair bonded and solitary individuals across eight socio-functional brain regions. We found that in females, ITR and V1aR receptor expression varied in the lateral septum-like region (the Vv/Vl), while in both sexes D1R, D2R, and MOR expression varied within the mesolimbic reward system, including a striatum-like region (the Vc); mirroring sites of action in M. ochrogaster. This study provides novel insights into the neurobiology of teleost pair bonding. It also reveals high convergence in the neurochemical mechanisms governing pair bonding across actinopterygians and sarcopterygians, by repeatedly co-opting and similarly assembling deep neurochemical and neuroanatomical homologies that originated in ancestral osteithes.
  • DNA methylation regulates transcriptional homeostasis of algal endosymbiosis in the coral model Aiptasia

    Li, Yong; Liew, Yi Jin; Cui, Guoxin; Cziesielski, Maha Joana; Zahran, Noura Ibrahim Omar; Michell, Craig T; Voolstra, Christian R.; Aranda, Manuel (Cold Spring Harbor Laboratory, 2017-11-03) [Preprint]
    The symbiotic relationship between cnidarians and dinoflagellates is the cornerstone of coral reef ecosystems. Although research is focusing on the molecular mechanisms underlying this symbiosis, the role of epigenetic mechanisms, which have been implicated in transcriptional regulation and acclimation to environmental change, is unknown. To assess the role of DNA methylation in the cnidarian-dinoflagellate symbiosis, we analyzed genome-wide CpG methylation, histone associations, and transcriptomic states of symbiotic and aposymbiotic anemones in the model system Aiptasia. We find methylated genes are marked by histone H3K36me3 and show significant reduction of spurious transcription and transcriptional noise, revealing a role of DNA methylation in the maintenance of transcriptional homeostasis. Changes in DNA methylation and expression show enrichment for symbiosis-related processes such as immunity, apoptosis, phagocytosis recognition and phagosome formation, and unveil intricate interactions between the underlying pathways. Our results demonstrate that DNA methylation provides an epigenetic mechanism of transcriptional homeostasis during symbiosis.
  • Widespread hybridization and bidirectional introgression in sympatric species of coral reef fish

    Harrison, Hugo B.; Berumen, Michael L.; Saenz-Agudelo, Pablo; Salas, Eva; Williamson, David H.; Jones, Geoffrey P. (Molecular Ecology, Wiley, 2017-10-28) [Article]
    Coral reefs are highly diverse ecosystems, where numerous closely related species often coexist. How new species arise and are maintained in these high geneflow environments have been long-standing conundrums. Hybridization and patterns of introgression between sympatric species provide a unique insight into the mechanisms of speciation and the maintenance of species boundaries. In this study, we investigate the extent of hybridization between two closely related species of coral reef fish: the common coral trout (Plectropomus leopardus) and the bar-cheek coral trout (Plectropomus maculatus). Using a complementary set of 25 microsatellite loci, we distinguish pure genotype classes from first- and later-generation hybrids, identifying 124 interspecific hybrids from a collection of 2,991 coral trout sampled in inshore and mid-shelf reefs of the southern Great Barrier Reef. Hybrids were ubiquitous among reefs, fertile and spanned multiple generations suggesting both ecological and evolutionary processes are acting to maintain species barriers. We elaborate on these finding to investigate the extent of genomic introgression and admixture from 2,271 SNP loci recovered from a ddRAD library of pure and hybrid individuals. An analysis of genomic clines on recovered loci indicates that 261 SNP loci deviate from a model of neutral introgression, of which 132 indicate a pattern of introgression consistent with selection favouring both hybrid and parental genotypes. Our findings indicate genome-wide, bidirectional introgression between two sympatric species of coral reef fishes and provide further support to a growing body of evidence for the role of hybridization in the evolution of coral reef fishes.
  • Recent expansion of heat-activated retrotransposons in the coral symbiont Symbiodinium microadriaticum

    Chen, Jit Ern; Cui, Guoxin; Wang, Xin; Liew, Yi Jin; Aranda, Manuel (The ISME Journal, Springer Nature, 2017-10-20) [Article]
    Rising sea surface temperature is the main cause of global coral reef decline. Abnormally high temperatures trigger the breakdown of the symbiotic association between corals and their photosynthetic symbionts in the genus Symbiodinium. Higher genetic variation resulting from shorter generation times has previously been proposed to provide increased adaptability to Symbiodinium compared to the host. Retrotransposition is a significant source of genetic variation in eukaryotes and some transposable elements are specifically expressed under adverse environmental conditions. We present transcriptomic and phylogenetic evidence for the existence of heat stress-activated Ty1-copia-type LTR retrotransposons in the coral symbiont Symbiodinium microadriaticum. Genome-wide analyses of emergence patterns of these elements further indicate recent expansion events in the genome of S. microadriaticum. Our findings suggest that acute temperature increases can activate specific retrotransposons in the Symbiodinium genome with potential impacts on the rate of retrotransposition and the generation of genetic variation under heat stress.The ISME Journal advance online publication, 20 October 2017; doi:10.1038/ismej.2017.179.
  • Ruegeria profundi sp. nov. and Ruegeria marisrubri sp. nov., isolated from the brine–seawater interface at Erba Deep in the Red Sea

    Zhang, Guishan; Haroon, Mohamed; Zhang, Ruifu; Dong, Xiaoyan; Wang, Dandan; Liu, Yunpeng; Xun, Weibing; Dong, Xiuzhu; Stingl, Ulrich (International Journal of Systematic and Evolutionary Microbiology, Microbiology Society, 2017-10-12) [Article]
    Two moderately halophilic marine bacterial strains of the family Rhodobacteraceae, designated ZGT108T and ZGT118T, were isolated from the brine-seawater interface at Erba Deep in the Red Sea (Saudi Arabia). Cells of both strains were aerobic, rod-shaped, non-motile, and Gram-stain-negative. The sequence similarity of the 16S rRNA genes of strains ZGT108T and ZGT118T was 94.9 %. The highest 16S rRNA gene sequence similarity of strain ZGT108T to its closest relative, Ruegeria conchae JCM 17315T, was 98.9 %, while the 16S rRNA gene of ZGT118T was most closely related to that of Ruegeria intermedia LMG 25539T (97.7 % similarity). The sizes of the draft genomes as presented here are 4 258 055 bp (strain ZGT108T) and 4 012 109 bp (strain ZGT118T), and the G+C contents of the draft genomes are 56.68 mol% (ZGT108T) and 62.94 mol% (ZGT108T). The combined physiological, biochemical, phylogenetic and genotypic data supported placement of both strains in the genus Ruegeria and indicated that the two strains are distinct from each other as well as from all other members in the genus Ruegeria. This was also confirmed by low DNA-DNA hybridization values (<43.6 %) and low ANI values (<91.8 %) between both strains and the most closely related Ruegeria species. Therefore, we propose two novel species in the genus Ruegeria to accommodate these novel isolates: Ruegeriaprofundi sp. nov. (type strain ZGT108T=JCM 19518T=ACCC 19861T) and Ruegeriamarisrubri sp. nov. (type strain ZGT118T=JCM 19519T= ACCC 19862T).
  • Ponticoccus marisrubri sp. nov., a moderately halophilic marine bacterium of the family Rhodobacteraceae

    Zhang, Guishan; Haroon, Mohamed; Zhang, Ruifu; Dong, Xiaoyan; Liu, Di; Xiong, Qin; Xun, Weibing; Dong, Xiuzhu; Stingl, Ulrich (International Journal of Systematic and Evolutionary Microbiology, Microbiology Society, 2017-10-06) [Article]
    Strain SJ5A-1T, a Gram-stain-negative, coccus-shaped, non-motile, aerobic bacterium, was isolated from the brine-seawater interface of the Erba Deep in the Red Sea, Saudi Arabia. The colonies of strain SJ5A-1T have a beige to pale-brown pigmentation, are approximately 0.5-0.7 µm in diameter, and are catalase and oxidase positive. Growth occurred optimally at 30-33 °C, pH 7.0-7.5, and in the presence of 9.0-12.0 % NaCl (w/v). Phylogenetic analysis of the 16S rRNA gene indicates that strain SJ5A-1T is a member of the genus Ponticoccus within the family Rhodobacteraceae. Ponticoccus litoralis DSM 18986T is the most closely related described species based on 16S rRNA gene sequence identity (96.7 %). The DNA-DNA hybridization value between strain SJ5A-1T and P. litoralis DSM 18986T was 36.7 %. The major respiratory quinone of strain SJ5A-1T is Q-10; it predominantly uses the fatty acids C18 : 1 (54.2 %), C18 : 0 (11.2 %), C16 : 0 (8.6 %), 11-methyl C18 : 1ω7c (7.7 %), C19 : 0cyclo ω8c (3.3 %), and C12 : 1 3-OH (3.5 %), and its major polar lipids are phosphatidylethanolamine, phosphatidylglycerol, phosphocholine, an unknown aminolipid, an unknown phospholipid and two unknown lipids. The genome draft of strain SJ5A-1T as presented here is 4 562 830 bp in size and the DNA G+C content is 68.0 mol %. Based on phenotypic, phylogenetic and genotypic data, strain SJ5A-1T represents a novel species in the genus Ponticoccus, for which we propose the name Ponticoccus marisrubri sp. nov. The type strain of P. marisrubri is SJ5A-1T (=JCM 19520T=ACCC19863T).
  • Symbiodinium genomes reveal adaptive evolution of functions related to symbiosis

    Liu, Huanle; Stephens, Timothy G.; González-Pech, Raúl; Beltran, Victor H.; Lapeyre, Bruno; Bongaerts, Pim; Cooke, Ira; Bourne, David G.; Forêt, Sylvain; Miller, David John; van Oppen, Madeleine J. H.; Voolstra, Christian R.; Ragan, Mark A.; Chan, Cheong Xin (Cold Spring Harbor Laboratory, 2017-10-06) [Preprint]
    Symbiosis between dinoflagellates of the genus Symbiodinium and reef-building corals forms the trophic foundation of the world's coral reef ecosystems. Here we present the first draft genome of Symbiodinium goreaui (Clade C, type C1: 1.03 Gbp), one of the most ubiquitous endosymbionts associated with corals, and an improved draft genome of Symbiodinium kawagutii (Clade F, strain CS-156: 1.05 Gbp), previously sequenced as strain CCMP2468, to further elucidate genomic signatures of this symbiosis. Comparative analysis of four available Symbiodinium genomes against other dinoflagellate genomes led to the identification of 2460 nuclear gene families that show evidence of positive selection, including genes involved in photosynthesis, transmembrane ion transport, synthesis and modification of amino acids and glycoproteins, and stress response. Further, we identified extensive sets of genes for meiosis and response to light stress. These draft genomes provide a foundational resource for advancing our understanding Symbiodinium biology and the coral-algal symbiosis.
  • Testing the Metabolic Theory of Ecology with marine bacteria: Different temperature sensitivity of major phylogenetic groups during the spring phytoplankton bloom

    Arandia-Gorostidi, Nestor; Huete-Stauffer, Tamara; Alonso-Sáez, Laura; Moran, Xose Anxelu G. (Environmental Microbiology, Wiley, 2017-10-02) [Article]
    Although temperature is a key driver of bacterioplankton metabolism, the effect of ocean warming on different bacterial phylogenetic groups remains unclear. Here, we conducted monthly short-term incubations with natural coastal bacterial communities over an annual cycle to test the effect of experimental temperature on the growth rates and carrying capacities of four phylogenetic groups: SAR11, Rhodobacteraceae, Gammaproteobacteria and Bacteroidetes. SAR11 was the most abundant group year-round as analysed by CARD-FISH, with maximum abundances in summer, while the other taxa peaked in spring. All groups, including SAR11, showed high temperature-sensitivity of growth rates and/or carrying capacities in spring, under phytoplankton bloom or post-bloom conditions. In that season, Rhodobacteraceae showed the strongest temperature response in growth rates, estimated here as activation energy (E, 1.43 eV), suggesting an advantage to outcompete other groups under warmer conditions. In summer E values were in general lower than 0.65 eV, the value predicted by the Metabolic Theory of Ecology (MTE). Contrary to MTE predictions, carrying capacity tended to increase with warming for all bacterial groups. Our analysis confirms that resource availability is key when addressing the temperature response of heterotrophic bacterioplankton. We further show that even under nutrient-sufficient conditions, warming differentially affected distinct bacterioplankton taxa. This article is protected by copyright. All rights reserved.
  • Genome based analyses of six hexacorallian species reject the “naked coral” hypothesis

    Wang, Xin; Drillon, Guénola; Ryu, Taewoo; Voolstra, Christian R.; Aranda, Manuel (Genome Biology and Evolution, Oxford University Press (OUP), 2017-09-25) [Article]
    Scleractinian corals are the foundation species of the coral-reef ecosystem. Their calcium carbonate skeletons form extensive structures that are home to millions of species, making coral reefs one of the most diverse ecosystems of our planet. However, our understanding of how reef-building corals have evolved the ability to calcify and become the ecosystem builders they are today is hampered by uncertain relationships within their subclass Hexacorallia. Corallimorpharians have been proposed to originate from a complex scleractinian ancestor that lost the ability to calcify in response to increasing ocean acidification, suggesting the possibility for corals to lose and gain the ability to calcify in response to increasing ocean acidification. Here we employed a phylogenomic approach using whole-genome data from six hexacorallian species to resolve the evolutionary relationship between reef-building corals and their non-calcifying relatives. Phylogenetic analysis based on 1,421 single-copy orthologs, as well as gene presence/absence and synteny information, converged on the same topologies, showing strong support for scleractinian monophyly and a corallimorpharian sister clade. Our broad phylogenomic approach using sequence-based and sequence-independent analyses provides unambiguous evidence for the monophyly of scleractinian corals and the rejection of corallimorpharians as descendants of a complex coral ancestor.
  • Excess labile carbon promotes the expression of virulence factors in coral reef bacterioplankton

    Cardenas, Anny; Neave, Matthew J.; Haroon, Mohamed; Pogoreutz, Claudia; Radecker, Nils; Wild, Christian; Gärdes, Astrid; Voolstra, Christian R. (The ISME Journal, Springer Nature, 2017-09-12) [Article]
    Coastal pollution and algal cover are increasing on many coral reefs, resulting in higher dissolved organic carbon (DOC) concentrations. High DOC concentrations strongly affect microbial activity in reef waters and select for copiotrophic, often potentially virulent microbial populations. High DOC concentrations on coral reefs are also hypothesized to be a determinant for switching microbial lifestyles from commensal to pathogenic, thereby contributing to coral reef degradation, but evidence is missing. In this study, we conducted ex situ incubations to assess gene expression of planktonic microbial populations under elevated concentrations of naturally abundant monosaccharides (glucose, galactose, mannose, and xylose) in algal exudates and sewage inflows. We assembled 27 near-complete (>70%) microbial genomes through metagenomic sequencing and determined associated expression patterns through metatranscriptomic sequencing. Differential gene expression analysis revealed a shift in the central carbohydrate metabolism and the induction of metalloproteases, siderophores, and toxins in Alteromonas, Erythrobacter, Oceanicola, and Alcanivorax populations. Sugar-specific induction of virulence factors suggests a mechanistic link for the switch from a commensal to a pathogenic lifestyle, particularly relevant during increased algal cover and human-derived pollution on coral reefs. Although an explicit test remains to be performed, our data support the hypothesis that increased availability of specific sugars changes net microbial community activity in ways that increase the emergence and abundance of opportunistic pathogens, potentially contributing to coral reef degradation.
  • Rapid adaptive responses to climate change in corals

    Torda, Gergely; Donelson, Jennifer M.; Aranda, Manuel; Barshis, Daniel J.; Bay, Line; Berumen, Michael L.; Bourne, David G.; Cantin, Neal; Foret, Sylvain; Matz, Mikhail; Miller, David J.; Moya, Aurelie; Putnam, Hollie M.; Ravasi, Timothy; van Oppen, Madeleine J. H.; Thurber, Rebecca Vega; Vidal-Dupiol, Jeremie; Voolstra, Christian R.; Watson, Sue-Ann; Whitelaw, Emma; Willis, Bette L.; Munday, Philip L. (Nature Climate Change, Springer Nature, 2017-09-01) [Article]
    Pivotal to projecting the fate of coral reefs is the capacity of reef-building corals to acclimatize and adapt to climate change. Transgenerational plasticity may enable some marine organisms to acclimatize over several generations and it has been hypothesized that epigenetic processes and microbial associations might facilitate adaptive responses. However, current evidence is equivocal and understanding of the underlying processes is limited. Here, we discuss prospects for observing transgenerational plasticity in corals and the mechanisms that could enable adaptive plasticity in the coral holobiont, including the potential role of epigenetics and coral-associated microbes. Well-designed and strictly controlled experiments are needed to distinguish transgenerational plasticity from other forms of plasticity, and to elucidate the underlying mechanisms and their relative importance compared with genetic adaptation.
  • Genomic diversification of giant enteric symbionts reflects host dietary lifestyles

    Ngugi, David; Miyake, Sou; Cahill, Matthew; Vinu, Manikandan; Hackmann, Timothy J.; Blom, Jochen; Tietbohl, Matthew; Berumen, Michael L.; Stingl, Ulrich (Proceedings of the National Academy of Sciences, Proceedings of the National Academy of Sciences, 2017-08-23) [Article]
    Herbivorous surgeonfishes are an ecologically successful group of reef fish that rely on marine algae as their principal food source. Here, we elucidated the significance of giant enteric symbionts colonizing these fishes regarding their roles in the digestive processes of hosts feeding predominantly on polysiphonous red algae and brown Turbinaria algae, which contain different polysaccharide constituents. Using metagenomics, single-cell genomics, and metatranscriptomic analyses, we provide evidence of metabolic diversification of enteric microbiota involved in the degradation of algal biomass in these fishes. The enteric microbiota is also phylogenetically and functionally simple relative to the complex lignocellulose-degrading microbiota of terrestrial herbivores. Over 90% of the enzymes for deconstructing algal polysaccharides emanate from members of a single bacterial lineage,
  • 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. (BMC Microbiology, Springer Nature, 2017-08-17) [Article]
    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.

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