The crown-of-thorns starfish genome as a guide for biocontrol of this coral reef pest

Abstract

The crown-of-thorns starfish (COTS, the Acanthaster planci species group) is a highly fecund predator of reef-building corals throughout the Indo-Pacific region 1 . COTS population outbreaks cause substantial loss of coral cover, diminishing the integrity and resilience of reef ecosystems 2-6 . 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.COTS are extremely fecund mass spawners 7 , which predisposes them to population outbreaks that result in a pronounced loss of live coral cover and associated biodiversity. These outbreaks have a higher impact on reef health and resilience than the combined effects of coral bleaching and disease, and increase the susceptibility of reefs to other potentially detrimental events, such as severe storms [2][3][4][5][6] (Supplementary Note 1).Although a range of local in situ control measures have been applied with some success (Supplementary Note 1), mitigation of COTS outbreaks on the necessary regional scale requires mass-deployed, species-specific strategies. In this context, genome-encoded COTSspecific attractants that underpin spawning aggregations have substantial potential as biocontrol agents. To identify attractants, we sequenced the genomes of two wild-caught individuals separated by over 5,000 km, one from the Great Barrier Reef (GBR), Australia and the other from Okinawa (OKI), Japan (Fig. 1c, d and Extended Data Fig. 1). We also sequenced transcriptomes from external organs, and proteins released into the seawater by COTS that were aggregating or were in the presence of their main predator, the giant triton Charonia tritonis (Fig. 1b).We generated separate 384 megabase (Mb) draft assemblies for the GBR and OKI genomes (Extended Data COTS genes are labelled and are marked with red lines; other asteroids, two shades of orange and yellow lines; sea urchins, dark green; hemichordates, light green; molluscs, pink; annelids, purple; cnidarians, black; and vertebrates, blue. The three clades to which COTS sequences belong are indicated by the outer circle. The asterisk denotes the fish-specific tru...

Thirty Years of Research on Crown-of-Thorns Starfish (1986–2016): Scientific Advances and Emerging Opportunities

“…This study found that CoTS contain proteins, molecules, signalling pathways and key developmental genes that are known to have a role in sperm motility and signalling in other echinoderms [263]. A recent study using genome sequencing and proteomics in combination with behavioral experiments, allowed the identification of key species-specific pheromones involved in their aggregation [176]. Although this result provides a potential solution to control adult populations of CoTS in the GBR, little is known about the molecular basis underlying CoTS life history stages in response to ecological factors.…”

“…Most notably, Vogler et al [38] sampled CoTS from the Red Sea to the eastern Pacific, and revealed at least four strongly differentiated clades, which has stimulated necessary research into the systematics and nomenclature [39] and raises many important questions about the biogeography of CoTS. Moreover, genomic data are providing unprecedented insights into the intrinsic mechanistic basis of CoTS behavior [176], providing new options for population control and management. It is these fields, along with advances in population modelling that are expected to advance understanding and management of CoTS outbreaks in coming years.…”

“…Predation may contribute to population regulation in several ways, including (i) direct reductions in the local densities of juvenile or adult CoTS; (ii) disrupting spawning aggregations [176]; (iii) reducing individual fecundity through partial predation (V. Messmer, unpublished data); and/or (iv) modifying settlement rates and behavior (Section 2.13). However, the initiation and spread of CoTS outbreaks cannot be definitively attributed to declines in the abundance of reef-based-predators, caused by sustained and on-going fishing (Section 2.22).…”

Persistent Gaps of Knowledge for Naming and Distinguishing Multiple Species of Crown-of-Thorns-Seastar in the Acanthaster planci Species Complex

“…However, the most recent publications on COTSs increasingly reflect the reception of the species complex and its implications (e.g., [18][19][20][21][22][23]). …”

The characterization of larval homology: transcriptomic insights into the origin and evolution of animal life cycles

“…Scaled values above zero indicate a domain abundance above the average across all species, which was used as a proxy for domain enrichment. Conversely, values below zero represent an underrepresented domain (Hall et al 2017). Sample correlation based on the presence/absence of protein domains was performed through the calculation of Euclidean distance using the DESeq2 R package (Love et al 2014).…”