1. Ecology
  2. Evolutionary Biology
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Comparative genomics explains the evolutionary success of reef-forming corals

  1. Debashish Bhattacharya  Is a corresponding author
  2. Shobhit Agrawal
  3. Manuel Aranda
  4. Sebastian Baumgarten
  5. Mahdi Belcaid
  6. Jeana L Drake
  7. Douglas Erwin
  8. Sylvian Foret
  9. Ruth D Gates
  10. David F Gruber
  11. Bishoy Kamel
  12. Michael P Lesser
  13. Oren Levy
  14. Yi Jin Liew
  15. Matthew MacManes
  16. Tali Mass
  17. Monica Medina
  18. Shaadi Mehr
  19. Eli Meyer
  20. Dana C Price
  21. Hollie M Putnam
  22. Huan Qiu
  23. Chuya Shinzato
  24. Eiichi Shoguchi
  25. Alexander J Stokes
  26. Sylvie Tambutté
  27. Dan Tchernov
  28. Christian R Voolstra
  29. Nicole Wagner
  30. Charles W Walker
  31. Andreas PM Weber
  32. Virginia Weis
  33. Ehud Zelzion
  34. Didier Zoccola
  35. Paul G Falkowski  Is a corresponding author
  1. Rutgers University, United States
  2. King Abdullah University of Science and Technology (KAUST), Saudi Arabia
  3. Hawaii Institute of Marine Biology, United States
  4. National Museum of Natural History, United States
  5. James Cook University, Australia
  6. Australian National University, Australia
  7. Sackler Institute for Comparative Genomics, United States
  8. City University of New York, Baruch College and The Graduate Center, United States
  9. Penn State University, United States
  10. University of New Hampshire, United States
  11. Bar-Ilan University, Israel
  12. University of Haifa, Israel
  13. State University of New York, College at Old Westbury, United States
  14. Oregon State University, United States
  15. Okinawa Institute of Science and Technology Graduate University, Japan
  16. John A. Burns School of Medicine, United States
  17. Chaminade University, United States
  18. Centre Scientifique de Monaco, Monaco
  19. Heinrich-Heine-Universität, Germany
Research Article
Cite this article as: eLife 2016;5:e13288 doi: 10.7554/eLife.13288
4 figures, 1 table, 21 data sets and 1 additional file

Figures

Multigene maximum likelihood (RAxML) tree inferred from an alignment of 391 orthologs (63,901 aligned amino acid positions) distributed among complete genome (boldface taxon names) and genomic data from 20 coral species and 12 outgroups.

The PROTGAMMALGF evolutionary model was used to infer the tree with branch support estimated with 100 bootstrap replicates. Robust and complex corals are shown in brown and green text, respectively, and non-coral metazoan species are shown in blue text.

https://doi.org/10.7554/eLife.13288.003
Figure 1—source data 1

Coral genomic data compiled in this study and their attributes.

https://doi.org/10.7554/eLife.13288.004
Figure 2 with 7 supplements
The mechanism of (A) coral biomineralization based on data from physiological and molecular approaches and (B) the major components of the human ion trafficking system that were identified in the coral genomic data (Figure 2—source data 1 for details).

Here, in (A) Biomineralization, 1 = carbonic anhydrases (orange); 2 = bicarbonate transporter (green); 3 = calcium-ATPase (purple); 4 = organic matrix proteins (shown as protein structures).

https://doi.org/10.7554/eLife.13288.005
Figure 2—source data 1

Major components of the human ion trafficking system identified in the coral genomic data.

https://doi.org/10.7554/eLife.13288.006
Figure 2—figure supplement 1
Bayesian consensus trees of SLC26.

Bayesian posterior probabilities are indicated when greater than 50%. For this analysis and for the trees shown in Figure 2—figure supplements 24, MrBayes v3.1.2 was used with a random starting tree and the LG model of amino acid substitution. Trees were generated for 6,000,000 generations and sampled every 1000 generations with four chains to obtain the consensus tree and to determine the posterior probabilities at the internal nodes.

https://doi.org/10.7554/eLife.13288.007
Figure 2—figure supplement 2
Bayesian consensus trees of SLC4.

Bayesian posterior probabilities (×100) are indicated when greater than 50%.

https://doi.org/10.7554/eLife.13288.008
Figure 2—figure supplement 3
Bayesian consensus trees of Cav.

Bayesian posterior probabilities (×100) are indicated when greater than 50%.

https://doi.org/10.7554/eLife.13288.009
Figure 2—figure supplement 4
Bayesian consensus trees of coral and outgroup Ca-ATPase proteins.

Bayesian posterior probabilities (×100) are indicated when greater than 50%.

https://doi.org/10.7554/eLife.13288.010
Figure 2—figure supplement 5
Evolution of CARPs and other coral acid-rich proteins.

(A) Maximum likelihood (RAxML) tree showing extensive history of duplication of genes encoding CARP 5 that predates the split of robust (brown text) and complex (green text) corals. (B) RAxML tree showing the origin of CARP 1 in robust (brown text) and complex (green text) corals from a reticulocalbin-like ancestor by the evolution of a novel acid-rich N-terminaldomain. The non-coral species in both trees are shown in blue text.

https://doi.org/10.7554/eLife.13288.011
Figure 2—figure supplement 6
Scatter plot of isoelectric points of collagens from Seriatopora, Stylophora, Nematostella, and Crassostrea gigas.
https://doi.org/10.7554/eLife.13288.012
Figure 2—figure supplement 7
Maximum likelihood (ML) trees of galaxin and amgalaxin.

(A) ML tree of best galaxin hits from 19 coral species (brown for robust corals and green for complex corals) and 11 non-coral species (blue text). (B) ML tree of best amgalaxin hits from 13 coral species. No outgroup blast hits were found against the acidic region of Acropora millepora amgalaxin 1 or 2 (Genbank accession numbers ADI50284.1 and ADI50285.1, respectively).

https://doi.org/10.7554/eLife.13288.013
Comparison of robust coral (brown text) and complex coral (green text) and non-coral (blue text) genomes with respect to percent of encoded proteins that contain either >30% or >40% negatively charged amino acid residues (i.e., aspartic acid [D] and glutamic acid [E]).

The average composition and standard deviation of D + E is shown for the two cut-offs of these estimates. On average, corals contain >2-fold more acidic residues than non-corals. This acidification of the coral proteome is postulated to result from the origin of biomineralization in this lineage.

https://doi.org/10.7554/eLife.13288.014
Figure 4 with 5 supplements
Analysis of a genomic region in Acropora digitifera that encodes a putative HGT candidate.

(A) The genome region showing the position of the HGT candidate (PNK3P) and its flanking genes. (B) Maximum likelihood trees of PNK3P (polynucleotide kinase 3 phosphatase, pfam08645) domain-containing protein and the proteins (RNA-binding and GTP-binding proteins) encoded by the flanking genes. Robust and complex corals are shown in brown and green text, respectively, and non-coral metazoan and choanoflagellate species are shown in blue text. Photosynthetic lineages, regardless of phylogenetic origin, are shown in magenta text and all other taxa are in black text. GenBank accession (GI) or other identifying numbers are shown for each sequence. The PNK3P domain plays a role in the repair of DNA single-strand breaks by removing single-strand 3'-end-blocking phosphates (Petrucco et al., 2002).

https://doi.org/10.7554/eLife.13288.015
Figure 4—figure supplement 1
Maximum likelihood trees of a DEAD-like helicase and the protein encoded by the flanking gene.

The bacterium-derived DEAD-like helicase genes in coral are nested within bacterial sequences, whereas the upstream host-derived gene (encoding mannosyl-oligosaccharide 1,2-alpha-mannosidase IB) is monophyletic with homologous genes from other metazoan species. The downstream Acropora digitifera-specific gene has no detectable homolog in other species. Robust and complex corals are shown in brown and green text, respectively, and non-coral metazoan and choanoflagellate species are shown in blue text. Photosynthetic lineages, regardless of phylogenetic origin, are shown in magenta text and all other taxa are in black text. GenBank accession (GI) or other identifying numbers are shown for each sequence.

https://doi.org/10.7554/eLife.13288.016
Figure 4—figure supplement 2
Maximum likelihood tree of an exonuclease-endonucease-phosphatase (EEP) domain-containing protein (A), an ATP-dependent endonuclease (B), a tyrosyl-DNA phosphodiesterase 2-like protein (C), and DNA mismatch repair (MutS-like) protein (D).

Robust and complex corals are shown in brown and green text, respectively, and non-coral metazoan and choanoflagellate species are shown in blue text. Photosynthetic lineages, regardless of phylogenetic origin, are shown in magenta text and all other taxa are in black text. GenBank accession (GI) or other identifying numbers are shown for each sequence.

https://doi.org/10.7554/eLife.13288.017
Figure 4—figure supplement 3
Maximum likelihood trees of glyoxalase I (or lactoylglutathione lyase) and the proteins encoded by the flanking genes (top image) in Acropora digitifera.

Robust and complex corals are shown in brown and green text, respectively, and non-coral metazoan and choanoflagellate species are shown in blue text. Photosynthetic lineages, regardless of phylogenetic origin, are shown in magenta text and all other taxa are in black text. GenBank accession (GI) or other identifying numbers are shown for each sequence.

https://doi.org/10.7554/eLife.13288.018
Figure 4—figure supplement 4
Maximum likelihood tree of a second glyoxalase I (or lactoylglutathione lyase) and the proteins encoded by the flanking genes (top image) in Acropora digitifera.

The coral glyoxalase gene gene was derived from a bacteria-specific gene type. Robust and complex corals are shown in brown and green text, respectively, and non-coral metazoan and choanoflagellate species are shown in blue text. Photosynthetic lineages, regardless of phylogenetic origin, are shown in magenta text and all other taxa are in black text. GenBank accession (GI) or other identifying numbers are shown for each sequence.

https://doi.org/10.7554/eLife.13288.019
Figure 4—figure supplement 5
Maximum likelihood tree of an algal-derived short-chain dehydrogenase/reductase (A), and a dinoflagellate-derived phosphonoacetaldehyde hydrolase (B).

Robust and complex corals are shown in brown and green text, respectively, and non-coral metazoan and choanoflagellate species are shown in blue text. Photosynthetic lineages, regardless of phylogenetic origin, are shown in magenta text and all other taxa are in black text. GenBank accession (GI) or other identifying numbers are shown for each sequence.

https://doi.org/10.7554/eLife.13288.020

Tables

Table 1

The list of non-redundant anthozoan genes derived via HGT.

https://doi.org/10.7554/eLife.13288.021
No.AncestorGenesProtein productsSupportSource(s)
1CoralA. digitifera_2036PNK3P100CA
2CoralA. digitifera_8849SDR100CA
3CoralSeriatopora_31861DEAD-like helicase100Bact
4CoralSeriatopora_16594glyoxalase100CA
5CoralSeriatopora_17147acyl- dehydrogenase100Bact
6CoralSeriatopora_17703carbonic anhydrase96Dino
7CoralSeriatopora_19477fatty acid or sphingolipid desaturase100CA
8CoralSeriatopora_3957atpase domain-containing protein100Bact
9CoralSeriatopora_7060sam domain-containing protein100Bact
10CoralSeriatopora_7928atp phosphoribosyltransferase100CA/Fungi
11CoralSeriatopora_8296glyoxalase98Bact
12CoralSeriatopora_225962-alkenal reductase92Bact
13CoralSeriatopora_28321histidinol-phosphate aminotransferase96Unclear
14AnthozoaA. digitifera_418duf718 domain protein100CA
15AnthozoaA. digitifera_15871peptidase s4996Algae/Bact
16AnthozoaA. digitifera_14520predicted protein100CA/Bact
17AnthozoaA. digitifera_7178rok family protein/fructokinase93Red algae
18AnthozoaA. digitifera_10592Phospholipid methyltransferase100CA/Viri
19AnthozoaA. digitifera_13390predicted protein100Bact
20AnthozoaA. digitifera_313malate synthase98CA/Bact
21AnthozoaA. digitifera_1537hypothetical protein100Bact
22AnthozoaA. digitifera_13577gamma-glutamyltranspeptidase 1-like100Unclear
23AnthozoaA. digitifera_5099Isocitrate lyase (ICL)100Bact
24AnthozoaA. digitifera_13467uncharacterized iron-regulated protein100CA
25AnthozoaA. digitifera_68663-dehydroquinate synthase98CA
26AnthozoaA. digitifera_11675intein c-terminal splicing region protein100Bact
27AnthozoaSeriatopora_10994penicillin amidase100Bact
28AnthozoaSeriatopora_14009nucleoside phosphorylase-like protein100Bact
29AnthozoaSeriatopora_14494phosphonoacetaldehyde hydrolase100Dino
30AnthozoaSeriatopora_15303exonuclease-endonuclease-phosphatase99CA/Viri
31AnthozoaSeriatopora_15772fmn-dependent nadh-azoreductase99Dino
32AnthozoaSeriatopora_19888had family hydrolase97Algae/Bact
33AnthozoaSeriatopora_20039chitodextrinase domain protein92Dino
34AnthozoaSeriatopora_20146glutamate dehydrogenase100CA/Bact
35AnthozoaSeriatopora_20479thif family protein100Bact
36AnthozoaSeriatopora_21195ATP-dependent endonuclease100Dino
37AnthozoaSeriatopora_8585chitodextrinase domain protein92Bact
38AnthozoaSeriatopora_24047aminotransferase100Bact
39AnthozoaSeriatopora_25961d-alanine ligase99Bact
40AnthozoaSeriatopora_26478quercetin 3-o-methyltransferase100Viri
41AnthozoaSeriatopora_29443diaminopimelate decarboxylase100CA
  1. Bact: Bacteria; CA: chlorophyll c-containing algae; Dino: dinoflagellates; Viri: Viridiplantae.

Data availability

The following previously published data sets were used
  1. 1
  2. 2
  3. 3
  4. 4
  5. 5
  6. 6
  7. 7
  8. 8
  9. 9
  10. 10
  11. 11
  12. 12
  13. 13
  14. 14
  15. 15
  16. 16
  17. 17
  18. 18
    Data from: A snapshot of a coral
    1. Shinzato C
    2. Inoue M
    3. Kusakabe M
    (2014)
    Publicly available at NCBI Bioproject (accession no. PRJDB731).
  19. 19
  20. 20
  21. 21

Additional files

Supplementary file 1

Taxonomic compilation and presence/absence in each taxon for genes involved in oxidative stress, DNA repair, cell cycle and apoptosis.

The values in parentheses show the number of taxa in which the gene sequence was recovered in the genomic database.

https://doi.org/10.7554/eLife.13288.022

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