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Mar Biotechnol (NY)
2021 Jun 01;233:501-515. doi: 10.1007/s10126-021-10042-7.
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Development and Interrogation of a Transcriptomic Resource for the Giant Triton Snail (Charonia tritonis).
Klein AH
,
Motti CA
,
Hillberg AK
,
Ventura T
,
Thomas-Hall P
,
Armstrong T
,
Barker T
,
Whatmore P
,
Cummins SF
.
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Gastropod molluscs are among the most abundant species that inhabit coral reef ecosystems. Many are specialist predators, along with the giant triton snail Charonia tritonis (Linnaeus, 1758) whose diet consists of Acanthaster planci (crown-of-thorns starfish), a corallivore known to consume enormous quantities of reef-building coral. C. tritonis are considered vulnerable due to overexploitation, and a decline in their populations is believed to have contributed to recurring A. planci population outbreaks. Aquaculture is considered one approach that could help restore natural populations of C. tritonis and mitigate coral loss; however, numerous questions remain unanswered regarding their life cycle, including the molecular factors that regulate their reproduction and development. In this study, we have established a reference C. tritonis transcriptome derived from developmental stages (embryo and veliger) and adult tissues. This was used to identify genes associated with cell signalling, such as neuropeptides and G protein-coupled receptors (GPCRs), involved in endocrine and olfactory signalling. A comparison of developmental stages showed that several neuropeptide precursors are exclusively expressed in post-hatch veligers and functional analysis found that FFamide stimulated a significant (20.3%) increase in larval heart rate. GPCRs unique to veligers, and a diversity of rhodopsin-like GPCRs located within adult cephalic tentacles, all represent candidate olfactory receptors. In addition, the cytochrome P450 superfamily, which participates in the biosynthesis and degradation of steroid hormones and lipids, was also found to be expanded with at least 91 genes annotated, mostly in gill tissue. These findings further progress our understanding of C. tritonis with possible application in developing aquaculture methods.
Fig. 1. Photos showing Charonia tritonis life stage. A Brooding female guarding recently laid intensely orange-coloured egg capsules. B A single yellow/opaque encapsulated larvae at 25 dpf. C A single encapsulated protoconch I larvae at 50 dpf. D A free-swimming veliger at 14 dph
Fig. 2. Charonia tritonis gene ontology (GO) annotation for developmental and adult tissues. dpf, days post-fertilisation; dph, days post-hatch; blue, cell compartment; yellow, molecular function; red, biological process
Fig. 3. Classification of G protein-coupled receptors (GPCRs) identified in Charonia tritonis into different families: glutamate, secretin, rhodopsin, cAMP neuropeptide-like and de novo. A GPCRs present at different stages of early life development: 25 days post-fertilisation (dpf), 50 dpf and 14 days post-hatch (dph). B Multiple sequence alignment of a GPCR exclusive to veligers at 14 dph (TRINITY_DN337635_c4_g1_i1) with a Mus musculus homolog GPCR. Blue shading represents conservation. C GPCRs present within different adult tissues. See Supplementary File S3 for all C. tritonis GPCR sequences
Fig. 4. Phylogenetic analysis of candidate olfactory receptors (ORs) identified in the cephalic tentacle of Charonia tritonis. Phylogenetic tree demonstrates the clustering of C. tritonis candidate ORs, represented by red, blue, green and orange clades. Aplysia californica candidate ORs are grouped into A, B and C
Fig. 5. Summary of neuropeptide precursor (NPP) genes present in Charonia tritonis.
A Graph showing NPP isoforms identified in early life development stages: 25 day post-fertilisation (dpf), 50 dpf and 14 day post-hatch (dph). B Summary of NPP genes present in adult tissues. Blue shading represents identified. See Supplementary File S3 for all Charonia tritonis NPP sequences
Fig. 6. Response of Charonia tritonis veliger heart rate (beats per minute; bpm) to chemical stimuli. Neuropeptides and serotonin were administered at 10 μM (n = 10). FSW, filtered seawater. *Significance is p < 0.05
Fig. 7. Summary of cytochrome P450 (CYP450) genes identified in Charonia tritonis and their functional classification. A Sequence logo representation showing conservation within CYP450 regions and motif. B CYP450 at different stages of early life development: 25 days post-fertilisation (dpf), 50 dpf and 14 days post-hatch (dph). C CYP450 within different adult tissues. See Supplementary File S3 for all Charonia tritonis CYP450 sequences
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