Comparative genomics explains the evolutionary success of reef-forming corals

Published on May 24, 2016in eLife 7.62
· DOI :10.7554/eLife.13288
Debashish Bhattacharya64
Estimated H-index: 64
(Rutgers University),
Shobhit Agrawal3
Estimated H-index: 3
(King Abdullah University of Science and Technology)
+ 32 AuthorsPaul G. Falkowski104
Estimated H-index: 104
(Rutgers University)
Abstract
For millions of years, reef-building stony corals have created extensive habitats for numerous marine plants and animals in shallow tropical seas. Stony corals consist of many small, tentacled animals called polyps. These polyps secrete a mineral called aragonite to create the reef – an external ‘skeleton’ that supports and protects the corals. Photosynthesizing algae live inside the cells of stony corals, and each species depends on the other to survive. The algae produce the coral’s main source of food, although they also produce some waste products that can harm the coral if they build up inside cells. If the oceans become warmer and more acidic, the coral are more likely to become stressed and expel the algae from their cells in a process known as coral bleaching. This makes the coral more likely to die or become diseased. Corals have survived previous periods of ocean warming, although it is not known how they evolved to do so. The evolutionary history of an organism can be traced by studying its genome – its complete set of DNA – and the RNA molecules encoded by these genes. Bhattacharya et al. performed this analysis for twenty stony coral species, and compared the resulting genome and RNA sequences with the genomes of other related marine organisms, such as sea anemones and sponges. In particular, Bhattacharya et al. examined “ortholog” groups of genes, which are present in different species and evolved from a common ancestral gene. This analysis identified the genes in the corals that encode the proteins responsible for constructing the aragonite skeleton. The coral genome also encodes a network of environmental sensors that coordinate how the polyps respond to temperature, light and acidity. Bhattacharya et al. also uncovered a variety of stress-related pathways, including those that detoxify the polyps of the damaging molecules generated by algae, and the pathways that enable the polyps to adapt to environmental stress. Many of these genes were recruited from other species in a process known as horizontal gene transfer. The oceans are expected to become warmer and more acidic in the coming centuries. Provided that humans do not physically destroy the corals’ habitats, the evidence found by Bhattacharya et al. suggests that the genome of the corals contains the diversity that will allow them to adapt to these new conditions.
  • References (113)
  • Citations (50)
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References113
Published on Jan 1, 2007in Methods of Molecular Biology
Emmanuel Boutet11
Estimated H-index: 11
(Swiss Institute of Bioinformatics),
Damien Lieberherr8
Estimated H-index: 8
(Swiss Institute of Bioinformatics)
+ 2 AuthorsAmos Marc Bairoch88
Estimated H-index: 88
(Swiss Institute of Bioinformatics)
The Swiss Institute of Bioinformatics (SIB), the European Bioinformatics Institute (EBI), and the Protein Information Resource (PIR) form the Universal Protein Resource (UniProt) consortium. Its main goal is to provide the scientific community with a central resource for protein sequences and functional information. The UniProt consortium maintains the UniProt KnowledgeBase (UniProtKB) and several supplementary databases including the UniProt Reference Clusters (UniRef) and the UniProt Archive (...
313 Citations Source Cite
Published on Jan 1, 2011in Advances in Marine Biology 2.23
Charles W. Walker23
Estimated H-index: 23
(University of New Hampshire),
Rebecca J. Van Beneden13
Estimated H-index: 13
(University of Maine)
+ 4 AuthorsW. Kelley Thomas33
Estimated H-index: 33
(University of New Hampshire)
Abstract The human p53 tumour suppressor protein is inactivated in many cancers and is also a major player in apoptotic responses to cellular stress. The p53 protein and the two other members of this protein family (p63, p73) are encoded by distinct genes and their functions have been extensively documented for humans and some other vertebrates. The structure and relative expression levels for members of the p53 superfamily have also been reported for most major invertebrate taxa. The functions ...
34 Citations Source Cite
Published on Jan 1, 2011
Zvy Dubinsky41
Estimated H-index: 41
,
Noga Stambler23
Estimated H-index: 23
History and perspective.- Geology and evolution.- Coral biology: symbiosis, photosynthesis and calcification.- The coral reef ecosystem: bacteria, zooplankton, algae, invertebrates, fishes and model.- Disturbances.- Conservation and management.
254 Citations Source Cite
Published on Dec 1, 2014in Environmental Microbiology 4.97
Elizabeth A. C. Heath-Heckman10
Estimated H-index: 10
(University of Wisconsin-Madison),
Amani Gillette4
Estimated H-index: 4
(University of Wisconsin-Madison)
+ 3 AuthorsMargaret J. McFall-Ngai51
Estimated H-index: 51
(University of Wisconsin-Madison)
Summary Most bacterial species make transitions between habitats, such as switching from free living to symbiotic niches. We provide evidence that a galaxin protein, EsGal1, of the squid Euprymna scolopes participates in both: (i) selection of the specific partner Vibrio fischeri from the bacterioplankton during symbiosis onset and, (ii) modulation of V. fischeri growth in symbiotic maintenance. We identified two galaxins in transcriptomic databases and showed by quantitative reverse-transcripta...
17 Citations Source Cite
Published on Aug 19, 2004in BMC Bioinformatics 2.21
Robert C. Edgar17
Estimated H-index: 17
(University of California, Berkeley)
Background In a previous paper, we introduced MUSCLE, a new program for creating multiple alignments of protein sequences, giving a brief summary of the algorithm and showing MUSCLE to achieve the highest scores reported to date on four alignment accuracy benchmarks. Here we present a more complete discussion of the algorithm, describing several previously unpublished techniques that improve biological accuracy and / or computational complexity. We introduce a new option, MUSCLE-fast, designed f...
4,154 Citations Source Cite
Published on Jan 1, 1996in The Journal of Experimental Biology 3.18
Eric Tambutté27
Estimated H-index: 27
,
Denis Allemand49
Estimated H-index: 49
+ 1 AuthorsJean Jaubert14
Estimated H-index: 14
Ca2+ compartments, Ca2+ transport and the calcification process were studied by using 45Ca as a tracer. The biological model used was clones of Stylophora pistillata developed into microcolonies whose skeleton is entirely covered by tissues, thus avoiding direct radioisotope exchange between the sea water and the skeleton. The study of Ca2+ compartments was performed by measuring two complementary parameters: Ca2+ influx and Ca2+ efflux kinetics. Kinetic analysis of 45Ca uptake revealed three ex...
151 Citations
Published on Feb 4, 2005in ChemBioChem 2.77
Bat‐Ami Gotliv2
Estimated H-index: 2
(Weizmann Institute of Science),
Naama Kessler16
Estimated H-index: 16
(Weizmann Institute of Science)
+ 4 AuthorsSteve Weiner79
Estimated H-index: 79
(Weizmann Institute of Science)
Almost all mineralized tissues contain proteins that are unusually acidic. As they are also often intimately associated with the mineral phase, they are thought to fulfill important functions in controlling mineral formation. Relatively little is known about these important proteins, because their acidic nature causes technical difficulties during purification and characterization procedures. Much effort has been made to overcome these problems, particularly in the study of mollusk-shell formati...
155 Citations Source Cite
Published on May 1, 2004in Biochimica et Biophysica Acta 3.44
Didier Zoccola28
Estimated H-index: 28
,
Eric Tambutté27
Estimated H-index: 27
+ 4 AuthorsSylvie Tambutté30
Estimated H-index: 30
Abstract Plasma-membrane calcium pumps (PMCAs) are responsible for the expulsion of Ca 2+ from the cytosol of all eukaryotic cells and are one of the major transport systems involved in long-term regulation of resting intracellular Ca 2+ concentration. An important feature of stony corals, one of the major groups of calcifying animals, is the continuous export of large quantities of Ca 2+ for skeletogenesis. Here, we report the cloning and functional expression of the stpPMCA gene from the coral...
109 Citations Source Cite
Published on Jan 1, 2013in BMC Genomics 3.73
Sebastian Baumgarten11
Estimated H-index: 11
(King Abdullah University of Science and Technology),
Till Bayer15
Estimated H-index: 15
(King Abdullah University of Science and Technology)
+ 4 AuthorsChristian R. Voolstra36
Estimated H-index: 36
(King Abdullah University of Science and Technology)
Background Animal and plant genomes produce numerous small RNAs (smRNAs) that regulate gene expression post-transcriptionally affecting metabolism, development, and epigenetic inheritance. In order to characterize the repertoire of endogenous smRNAs and potential gene targets in dinoflagellates, we conducted smRNA and mRNA expression profiling over 9 experimental treatments of cultures from Symbiodinium microadriaticum, a photosynthetic symbiont of scleractinian corals.
50 Citations Source Cite
Jeana L. Drake7
Estimated H-index: 7
,
Tali Mass12
Estimated H-index: 12
+ 3 AuthorsPaul G. Falkowski104
Estimated H-index: 104
(Rutgers University)
It has long been recognized that a suite of proteins exists in coral skeletons that is critical for the oriented precipitation of calcium carbonate crystals, yet these proteins remain poorly characterized. Using liquid chromatography-tandem mass spectrometry analysis of proteins extracted from the cell-free skeleton of the hermatypic coral, Stylophora pistillata, combined with a draft genome assembly from the cnidarian host cells of the same species, we identified 36 coral skeletal organic matri...
85 Citations Source Cite
Cited By50
Published on Jan 1, 2016in Database 3.98
Yi Jin Liew9
Estimated H-index: 9
,
Manuel Aranda23
Estimated H-index: 23
,
Christian R. Voolstra36
Estimated H-index: 36
We would like to thank the numerous labs that contributed data hosted on our website, and the three anonymous reviewers that helped improve our article. Research reported in this publication was supported by KAUST.
21 Citations Source Cite
Published on Dec 1, 2016in Scientific Reports 4.12
Manuel Aranda23
Estimated H-index: 23
(King Abdullah University of Science and Technology),
Yangyang Li1
Estimated H-index: 1
(King Abdullah University of Science and Technology)
+ 15 AuthorsVladimir B. Bajic45
Estimated H-index: 45
(King Abdullah University of Science and Technology)
Despite half a century of research, the biology of dinoflagellates remains enigmatic: they defy many functional and genetic traits attributed to typical eukaryotic cells. Genomic approaches to study dinoflagellates are often stymied due to their large, multi-gigabase genomes. Members of the genus Symbiodinium are photosynthetic endosymbionts of stony corals that provide the foundation of coral reef ecosystems. Their smaller genome sizes provide an opportunity to interrogate evolution and functio...
72 Citations Source Cite
Published on May 1, 2017in Cell and Tissue Research 3.04
M. Raz-Bahat1
Estimated H-index: 1
(National Institute of Oceanography, India),
Elizabeth Moiseeva7
Estimated H-index: 7
(National Institute of Oceanography, India)
+ 2 AuthorsB. Rinkevich12
Estimated H-index: 12
(National Institute of Oceanography, India)
Because hermatypic species use symbiotic algal photosynthesis, most of the literature in this field focuses on this autotrophic mode and very little research has studied the morphology of the coral’s digestive system or the digestion process of particulate food. Using histology and histochemestry, our research reveals that Stylophora pistillata’s digestive system is concentrated at the corals’ peristome, actinopharynx and mesenterial filaments (MF). We used in-situ hybridization (ISH) of the RNA...
4 Citations Source Cite
Published on Dec 1, 2017in BMC Molecular Biology 2.79
Gaurav G. Shimpi2
Estimated H-index: 2
(Ludwig Maximilian University of Munich),
Sergio Vargas8
Estimated H-index: 8
(Ludwig Maximilian University of Munich)
+ 1 AuthorsGert Wörheide40
Estimated H-index: 40
(Ludwig Maximilian University of Munich)
Background Mitogenome diversity is staggering among early branching animals with respect to size, gene density, content and order, and number of tRNA genes, especially in cnidarians. This last point is of special interest as tRNA cleavage drives the maturation of mitochondrial mRNAs and is a primary mechanism for mt-RNA processing in animals. Mitochondrial RNA processing in non-bilaterian metazoans, some of which possess a single tRNA gene in their mitogenomes, is essentially unstudied despite i...
3 Citations Source Cite
Published on Jan 1, 2017in Genome Biology and Evolution 3.94
Mei-Fang Lin4
Estimated H-index: 4
(James Cook University),
Aurelie Moya16
Estimated H-index: 16
(James Cook University)
+ 5 AuthorsDavid S. Miller70
Estimated H-index: 70
(James Cook University)
Corallimorpharians (coral-like anemones) have a close phylogenetic relationship with scleractinians (hard corals) and can potentially provide novel perspectives on the evolution of biomineralization within the anthozoan subclass Hexacorallia. A survey of the transcriptomes of three representative corallimorpharians led to the identification of homologs of some skeletal organic matrix proteins (SOMPs) previously considered to be restricted to corals. Carbonic anhydrases (CAs), which are ubiquitou...
3 Citations Source Cite
Published on Feb 15, 2017in PLOS ONE 2.77
Davide Poli1
Estimated H-index: 1
,
Elena Fabbri29
Estimated H-index: 29
+ 2 AuthorsSilvia Franzellitti17
Estimated H-index: 17
4 Citations Source Cite
Published on Feb 1, 2017in Science Advances
Pim Bongaerts21
Estimated H-index: 21
(University of Queensland),
Cynthia Riginos27
Estimated H-index: 27
(University of Queensland)
+ 3 AuthorsOve Hoegh-Guldberg79
Estimated H-index: 79
(University of Queensland)
Deep coral reefs (that is, mesophotic coral ecosystems) can act as refuges against major disturbances affecting shallow reefs. It has been proposed that, through the provision of coral propagules, such deep refuges may aid in shallow reef recovery; however, this "reseeding" hypothesis remains largely untested. We conducted a genome-wide assessment of two scleractinian coral species with contrasting reproductive modes, to assess the potential for connectivity between mesophotic (40 m) and shallow...
42 Citations Source Cite
Published on Mar 7, 2017in Frontiers in Microbiology 4.02
Raquel S. Peixoto28
Estimated H-index: 28
(Federal University of Rio de Janeiro),
Phillipe M. Rosado1
Estimated H-index: 1
(Federal University of Rio de Janeiro)
+ 2 AuthorsDavid G. Bourne45
Estimated H-index: 45
(James Cook University)
The symbiotic association between the coral animal and its endosymbiotic dinoflagellate partner Symbiodinium is central to the success of corals. However, an array of other microorganisms associated with coral (i.e., Bacteria, Archaea, Fungi and viruses) have a complex and intricate role in maintaining homeostasis between corals and Symbiodinium. Corals are sensitive to shifts in the surrounding environmental conditions. One of the most widely reported responses of coral to stressful environment...
38 Citations Source Cite
Published on Jan 1, 2017in Invertebrate Systematics 1.65
Christian R. Voolstra36
Estimated H-index: 36
(King Abdullah University of Science and Technology),
Gert Wörheide40
Estimated H-index: 40
(Ludwig Maximilian University of Munich),
Jose V. Lopez22
Estimated H-index: 22
(UPRRP College of Natural Sciences)
The Global Invertebrate Genomics Alliance (GIGA), a collaborative network of diverse scientists, marked its second anniversary with a workshop in Munich, Germany in 2015, where international attendees focused on discussing current progress, milestones and bioinformatics resources. The community determined the recruitment and training of talented researchers as one of the most pressing future needs and identified opportunities for network funding. GIGA also promotes future research efforts to pri...
4 Citations Source Cite
Published on Jun 1, 2017in Molecular Phylogenetics and Evolution 4.41
Zac H. Forsman15
Estimated H-index: 15
,
Ingrid S. Knapp8
Estimated H-index: 8
+ 3 AuthorsRobert J. Toonen8
Estimated H-index: 8
Abstract Major gaps remain in our understanding of the ecology, evolution, biodiversity, biogeography, extinction risk, and adaptive potential of reef building corals. One of the central challenges remains that there are few informative genetic markers for studying boundaries between species, and variation within species. Reduced representation sequencing approaches, such as RADseq (Restriction site Associated DNA sequencing) have great potential for resolving such relationships. However, it is ...
7 Citations Source Cite