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iScience
2025 Mar 18;284:112161. doi: 10.1016/j.isci.2025.112161.
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A family of crown-of-thorns starfish spine-secreted proteins modify adult conspecific behavior.
Harris RJ
,
Hillberg AK
,
Bastin LD
,
Lausen BS
,
Suwansa-Ard S
,
Wang T
,
Elizur A
,
Kikuchi S
,
Nakashima K
,
Satoh N
,
Motti CA
,
Cummins SF
.
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With growing interest in utilizing semiochemicals to control pest species, recent investigations have begun to consider semiochemicals to control outbreaks of crown-of-thorns starfish (CoTS; Acanthaster cf. solaris), a corallivore contributing to coral reef degradation. In this study, differential gene expression analysis of adult CoTS spines led to the identification of (1) numerous G-protein coupled receptor genes enriched at the reproductive stage, possibly reflecting enhanced sensitivity to semiochemicals and (2) genes encoding secreted proteins at the non-reproductive stage. We also demonstrated that these proteins belong to an uncharacterized family of secreted proteins that are unique to Acanthaster spp., being released into the surrounding water. A synthetic peptide mixture derived from this protein family demonstrated no toxicity yet did modify conspecific adult behavior, eliciting attraction. Based on this evidence, we suggest a pheromonal role beyond reproduction. The discovery of these provides a tool for future innovative semiochemical biocontrol in CoTS management strategies.
Figure 1. Differential gene expression of crown-of-thorns starfish (CoTS; Acanthaster spp. complex omitting A. brevispinus) spine tissue between reproductive and non-reproductive stages(A) Volcano plot shows significant (sig. -Log10 > 2.2; Log2 fold change (FC) between -1.8 and 1.8) differentially expressed genes, including table with top hits based on FC and significance labeled with gene identifier. All gene IDs are based on CoTS oki (Okinawa) genes. Tables show the top 10 DEGs based on highest FC.(B) Graph showing biological function GO annotation of all significantly upregulated genes at reproductive stage.(C) Graph showing biological function GO annotation of all significantly upregulated genes at non-reproductive stage.
Figure 2. Annotation and expression (based on Log2 value) of significantly upregulated receptors within crown-of-thorns starfish (CoTS) spine tissue at the reproductive stageThe color scale represents the level of CoTS gene expression: high = red, medium = clear, and low = blue. For raw transcripts per million (TPM) gene expression values, see Table S1.
Figure 3. Comparative protein sequence and tissue expression(A) Multiple sequence alignment of seven forms of the crown-of-thorns starfish (CoTS) spine-secreted proteins, as well as Acanthaster brevispinus homologs (Abrev1, 2). Asterisks indicates predicted cleavage sites.(B) Graph comparing gene expression across various CoTS tissues: spine reproductive (R), spine non-reproductive (NR), stomach, radial nerve cord (RNC), tube foot (TF) and sensory tentacle (ST). Asterisks indicate significant difference (p < 0.05) between R and NR spines.
Figure 4. Toxicity and behavioral assays to assess the crown-of-thorns starfish (CoTS) synthetic peptide mixture (SPM)(A) Brine shrimp (Artemia salina) lethality assay (n = 14 A. salina/well) to assess toxicity of the CoTS SPM (n = 5 replicates per concentration). Behavioral response of CoTS to SPM. A two-way ANOVA was used to test significance.(B) Cumulative heatmaps from dual flumes showing attraction of CoTS to the SPM (n = 14; n = 9 left flume and n = 5 right flume—the white dots on either side of the cue arm indicate where the source of the SPM was fed into each respective cue arm.(C) Combined meandering (deg/cm) when exposed to control (n = 15) and SPM at 1 nM (n = 14).(D) Combined time spent in arm (s) when exposed to control (n = 15) and CoTS SPM at 1 nM (n = 14). An independent samples t test was used to test significance with a threshold of p < 0.01 indicated by an asterisk.
