The crown-of-thorns starfish (COTS, the Acanthaster planci species group) is a highly fecund predator of reef-building corals throughout the Indo-Pacific region1. COTS population outbreaks cause substantial loss of coral cover, diminishing the integrity and resilience of reef ecosystems2, 3, 4, 5, 6. Here we sequenced genomes of COTS from the Great Barrier Reef, Australia and Okinawa, Japan to identify gene products that underlie species-specific communication and could potentially be used in biocontrol strategies. We focused on water-borne chemical plumes released from aggregating COTS, which make the normally sedentary starfish become highly active. Peptide sequences detected in these plumes by mass spectrometry are encoded in the COTS genome and expressed in external tissues. The exoproteome released by aggregating COTS consists largely of signalling factors and hydrolytic enzymes, and includes an expanded and rapidly evolving set of starfish-specific ependymin-related proteins. These secreted proteins may be detected by members of a large family of olfactory-receptor-like G-protein-coupled receptors that are expressed externally, sometimes in a sex-specific manner. This study provides insights into COTS-specific communication that may guide the generation of peptide mimetics for use on reefs with COTS outbreaks.
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Extended data figures and tables
Extended Data Figures
- Extended Data Figure 1: Deuterostome phylogeny showing placement of Acanthaster within asteroids. (511 KB)
A concatenated supermatrix of 427 genes (95,585 amino acids, 45.16% missing data) recovering a fully resolved tree. With exception of support for hemichordate monophyly (bootstrap support value = 98%), we found maximal support for all phylum- and class-level taxa. Species sampled, annotations and characteristics of each gene analysed are presented in Supplementary Note 4. Bootstrap support values below 100 are shown. Scale bar: 0.1 substitutions per site.
- Extended Data Figure 2: Acanthaster planci heterozygosity. (104 KB)
a, Single-nucleotide polymorphism (SNP) analysis showing the number of SNPs identified within and between OKI and GBR genomes. Percentage heterozygosity within these genomes and the level of nucleotide variance between genomes are shown. See Supplementary Note 2 for further details. b, k-mer (17-mer) plot. The GBR (green) and OKI (red) genomes were estimated to be 441 and 421 Mb, respectively.
- Extended Data Figure 3: Pfam enrichment in the genomes of selected metazoans displayed as relative abundance heat maps. (438 KB)
a, Comparison of metazoans. b, Comparison of deuterostomes. c, Comparison of ambulacrarians. See Supplementary Note 5 for further details of methods and analyses.
- Extended Data Figure 4: Comparison of Hox clusters. (883 KB)
a, Genome browser views of the Hox cluster on GBR scaffold 27 and OKI scaffold 15. Stylised Hox clusters are shown below each scaffold with the corresponding gene model for each Hox gene identified on the scaffold. b, Table of OKI and GBR Hox gene models. Prefix corresponds to scaffold. c, Micro-synteny of Hox cluster-containing OKI scaffold 15 and GBR scaffolds 27, 51 and 25. d, Mapping of OKI and GBR scaffolds containing the Hox cluster to each other. e, Molecular phylogenetic analysis of select bilaterian Hox genes by the maximum-likelihood method. Bootstrap support values over 50% are shown. Scale bar: 0.2 substitutions per site. Species abbreviations: Bfl, Branchiostoma floridae; Dme, Drosophila melanogaster; oki.scaffold.genemodel, A. planci OKI; Pfl, Ptychodera flava; Sko, Saccoglossus kowalevskii; and Spu, Stronglocentrotus purpuratus.
- Extended Data Figure 5: Response of crown-of-thorns starfish to seawater conditioned with its predator the giant triton, Charonia tritonis. (283 KB)
a, Top, diagram showing Y-maze experimental design showing arm dividers and starter zones (yellow). Middle, heat maps showing the cumulative response of COTS over 45 min to water conditioned with a giant triton (left) and ambient seawater (right) (n = 18). Red, area in which COTS spent most of the time with descending time to blue; black, no presence. Green outline represents the Y-maze and arm divider that prevents recirculation of water into the opposite arm; starter zones are demarcated by yellow lines. b, The duration of movement (highly active threshold set at >60%; t = −2.936, P = 0.006, 2-tailed t-test). c, The meander (change in direction of movement) of active animals over 45 min (t = 4.437, P = 0.000, 2-tailed t-test). Control, ambient seawater only; giant triton, ambient seawater conditioned with giant triton exudate. Mean ± s.e.m. See Supplementary Video 3 and Supplementary Note 7 for further details.
- Extended Data Figure 6: Protein classes in the crown-of-thorns starfish secretome. (197 KB)
a, Overall distribution of characterized secretome. b, Distribution of structural, signalling and unclassified proteins. c, Distribution of enzyme types.
- Extended Data Figure 7: Extended phylogeny of the EPDR proteins. (690 KB)
a, Phylogenetic tree of EPDRs incorporating those identified from ambulacrarian transcriptomes. COTS genes are indicated in red, those from non-COTS taxa within the order Valvatida in orange, from non-valvatid taxa within the class Asteroidea in yellow, and from non-asteroid taxa within the phylum Echinodermata in green. Branches with maximum-likelihood bootstrap values >70 and Bayesian posterior probability values >0.9 are indicated by a solid line; those with lower values are indicated by a dashed line. The scale bar indicates the number of substitutions per site. Major EPDR clades are indicated by numbers on the outer circle. Sequences used in the alignment can be found in Supplementary Note 8. b, Sequence logos constructed from the conserved region of sequences from each of the seven clades identified in a. The height of the amino acid residues indicates the level of conservation, residues highlighted in blue are highly conserved across all clades. Clade 1 is the most highly conserved EPDR clade (ultraconserved motifs are boxed). Clades 3–7 show much lower sequence conservation overall, and possess an extra pair of cysteine residues (highlighted in red).
- Extended Data Figure 8: GPCR abundance, structure and expression in crown-of-thorns starfish. (225 KB)
a, Abundance of GPCR genes in ambulacrarians and amphioxus, showing the distribution of the five GPCR classes in each species. See Supplementary Note 9 for further details on genes and analyses. b, Tissue expression of each non-rhodopsin class GPCRs in COTS tissues. c, Additional examples of GPCR gene clusters in COTS, with genes in clades b, and f–h shown in Fig. 4b. All genes have one exon and are depicted as grey arrowheads that point in the direction of transcription. GBR scaffold numbers are shown above the line; scale bar, 20 kb.
Extended Data Tables
- Video 1: Response of crown-of-thorns starfish over 45 minutes to factors released by aggregating starfish. (1.03 MB, Download)
- Time-lapse videos of 45 min Y-maze behavioural assays showing in the first instance two crown-of-thorns starfish subjected to flowing ambient seawater (control) and then two different COTS subjected to flowing seawater conditioned with factors released by aggregating COTS. Two example Y-mazes are shown (1, 2), with right (R) and left (L) arms. 270x real time speed.
- Video 2: Response of crown-of-thorns starfish over 8 hours to factors released by aggregating starfish. (3.61 MB, Download)
- Time-lapse videos of 8 h Y-maze behavioural assays showing in the first instance two crown-of-thorns starfish subjected to flowing ambient seawater (control) and then two different COTS subjected to flowing seawater conditioned with factors released by aggregating COTS. Two example Y-mazes are shown (1, 2), with right (R) and left (L) arms. 480x real time speed.
- Video 3: Response of crown-of-thorns starfish over 45 minutes to factors released by their predator, the giant triton. (446 KB, Download)
- Time-lapse videos of 45 min Y-maze behavioural assays showing two crown-of-thorns starfish, one subjected to flowing ambient seawater (control) and the other subjected to flowing seawater conditioned with factors released by their predator, the giant triton. Two Y-mazes are shown (1, 2), with right (R) and left (L) arms. 270x real time speed.
- Supplementary Information (4.6 MB)
This file contains Supplementary Notes, Figures and additional references.
- Supplementary Tables (9.4 MB)
This zipped file contains Supplementary Tables S1-9 and a Supplementary Table guide.