Characterization of the neuropeptidome of a Southern Ocean decapod, the Antarctic shrimp Chorismus antarcticus: Focusing on a new decapod ITP-like peptide belonging to the CHH peptide family

doi:10.1016/j.ygcen.2017.07.015

General and Comparative Endocrinology

Volume 252, 1 October 2017, Pages 60-78

https://doi.org/10.1016/j.ygcen.2017.07.015 Get rights and content

Highlights

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Illumina sequencing was used to produce a transcriptome of Chorismus antarcticus.
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Analysis of the assembly produced 55 pre-pro-peptides coding for 111 neuropeptides.
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A new member of the CHH family blasting with ITP peptides was characterized.
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This new group of peptides would integrate with the set of type 2 CHH peptides.

Abstract

As part of the study of the resilience of Antarctic crustaceans to global warming, the shrimp Chorismus antarcticus was subjected to an analysis of global approach using the Next Generation Sequencing Illumina Hi-Seq platform. With this data a detailed study into the principal neuropeptides and neurohormones of this species have been undertaken. Total RNAs from whole animals were enriched with eyestalk extracts to ensure maximum sequencing depth of the different neurohormones and neuropeptides mainly expressed into the X organ-sinus gland complex, which is a major endocrine organ of their synthesis. Apart from the information that can provide the availability of the transcriptome of a polar crustacean, the study of neuropeptides of a caridean shrimp will partially fill the limited data available for this taxon. Illumina sequencing was used to produce a transcriptome of the polar shrimp. Analysis of the Trinity assembled contigs produced 55 pre-pro-peptides, coding for 111 neuropeptides belonging to the following families: adipokinetic-corazonin-like peptide, Allatostatins (A, B et C), Bursicon (α), CCHamide, Crustacean Hyperglycemic Hormones (CHH), Crustacean Cardioactive Peptide (CCAP), Corazonin, Crustacean Female Sex Hormone (CSFH), Diuretic Hormones 31 and 45 (DH), Eclosion Hormone (EH), FLRFamide, GSEFLamide, Intocin, Ion Transport Peptide-like (ITP-like), Leucokinin, Molt-inhibiting Hormone, Myosuppresin, Neuroparsin, Neuropeptide F (NPF), Orcokinin, Orcomyotropin, Pigment Dispersing Hormone (PDH), Pyrokinin, Red Pigment Concentrating Hormone (RPCH), SIFamide, small Neuropeptide F (sNPF), Sulfakinin and finally Tachykinin Related peptides. Among the new peptides highlighted in this study, the focus was placed on the peptides of the CHH family and more particularly on a new ITP-like in order to confirm its belonging to a new group of peptides of the family. A phylogeny made from more than 200 sequences of peptides, included new sequences from new species besides Chorismus antarcticus, confirms the peculiarity of this new set of peptides gathered under the name ITP-like.

Introduction

The scarcity of representatives of crustacean decapods in the Antarctic Ocean is one of the most surprising and enigmatic observations in the study of biodiversity (Gorny, 1999, Thatje and Arntz, 2004). This diversity is summed up by a dozen species of benthic caridean shrimps among which is the Antarctic shrimp Chorismus antarcticus. This small hippolytid shrimp only occurs on the continental shelf in depths shallower than 700 m (Arntz and Gorny, 1991, Basher et al., 2014). The presence of this shrimp on the bottom of the continental shelf suggests that, like other benthic invertebrates, it would be strictly stenothermal and therefore would possess a limited capacity to respond to a potential warming of waters (Peck, 2004, Peck et al., 2010, Portner et al., 2007).

As part of an ongoing study of the resilience of Antarctic crustaceans such as krill to global warming (Cascella et al., 2015), C. antarcticus seemed another good model because of its different life mode and its close phylogenetic position in relative to euphausiids. So, a similar global approach was taken in this study using the Next Generation Sequencing Illumina Hi-Seq platform. With this data a detailed study into the principal neuropeptides and neurohormones of this species have been undertaken. As with the ice krill Euphausia crystallorophias (Toullec et al., 2013), total RNAs from whole animals were enriched with eyestalk extracts to maximize sequencing depth of the different neurohormones and neuropeptides mainly expressed into the X organ-sinus gland complex, which is the major endocrine organ of their synthesis. Apart from the information that can provide the availability of the transcriptome of a polar crustacean, the study of neuropeptides of a caridean shrimp will partially fill the limited data available for this taxon. Indeed, paradoxically, few neuropeptides sequences are available outside of economically important species such as Macrobrachium sp. and there is not, to our knowledge, another transcriptomic analysis focusing on these neuropeptides except again on M. rosenbergii (Suwansa-Ard et al., 2015). Moreover, the characterization of an ITP-like sequence within this decapod species has represented the opportunity not only to deepen the reality of the existence of this new family of peptides in this taxon but also to make a point on the phylogeny of the CHH family in Euarthropods by incorporating a maximum of new sequences resulting from studies of recent peptidomes.

Section snippets

Materials and methods

This project (IPEV-1039) was approved by IPEV (Institut Paul Emile Victor, the French Polar Institute) review committee and was declared to and approved by the Terres Australes et Antarctiques Françaises in 2009 according the Annex I of the Madrid Protocol and the French Decree No 2005-403. No endangered or protected species were used.

RNAseq assemblies

A total of 102,119,756 paired-end raw reads with read lengths of 100 bp were generated. After data cleaning to remove adapters and poor quality parts, 100,923,981, high quality paired reads were obtained. Reads were deposited in Sequence Read Archive (SRA) under the references SRR5138508; SRR5138509.

Based on these high-quality reads, contigs were assembled into a first assembly of 275,284 transcripts (corresponding to 185,677 Trinity «genes») with lengths ranging from 201 to 24,080 bp, an average

Focus on CHH peptide family

In recent years, the multiplication of transcriptome explorations in an increasing number of crustaceans has allowed us to deepen our knowledge of peptidomes and particularly of the families of key peptides such as CHH. As mentioned above, the number of members of this family is steadily expanding with the result that our vision is seriously complicated and even undermines our understanding of the structural and functional diversity of these peptides. The aim of this section is to try to make a

Conclusions

Today, the study of the biology or physiology of a new species needs the primordial steps of sequencing and assembly of its transcriptome, thus constituting a true identity card. Besides the interest of identifying the potential actors of the main biological functions studied, the exploration of the transcriptome allows us to deepen our knowledge of the diversity and evolution of these same actors. The peptidome of Chorismus antarcticus does not escape this rule, especially because relatively

Acknowledgments

JYT would like to thank all the IPEV staff at the base Dumont d’Urville and especially A. Pottier for his help for fishing during different Antarctic campaigns in Terre Adélie. The authors are grateful to Philippe Bouchet, Laure Corbari and Sarah Samadi, expedition leaders of KAVIENG 2014, SALOMON2, MADEEP of the MNHN program Tropical Deep Sea Benthos, Marie-Anne Cambon-Bonavita, cruise leader of BICOSE 2014 and Stéphane Hourdez, for the biological material they provided from which

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Earlier attempts to isolate MIH from hermit crab and squat lobster failed, but distinct CHH- and MIH-immunoreactive perikarya were localized in the hermit crab ESG (Montagné et al., 2008). In addition to these Type-I and -II peptides, respectively, red king crab also expressed the Type-III ITP-like peptide, which has been reported in several malacostracan species (Manfrin et al., 2015; Toullec et al., 2017). The function of crustacean ITP-like is unknown, while a possible ecdysis-related function has been suggested for insect ITP, in addition to regulating water homeostasis (Dircksen, 2009).
Red king crab (Paralithodes camtschaticus) and snow crab (Chionoecetes opilio) are deep-sea crustaceans widely distributed in the North Pacific and Northwest Atlantic Oceans. These giant predators have invaded the Barents Sea over the past decades, and climate-driven temperature changes may influence their distribution and abundance in the sub-Arctic region. Molting and growth in crustaceans are strongly affected by temperature, but the underlying molecular mechanisms are little known, particularly in cold-water species. Here, we describe multiple regulatory factors in the two high-latitude crabs by developing de novo transcriptomes from the molting gland (Y-organ or YO) and eye stalk ganglia (ESG), in addition to the hepatopancreas and claw muscle of red king crab. The Halloween genes encoding the ecdysteroidogenic enzymes were expressed in YO, and the ESG contained multiple neuropeptides, including molt-inhibiting hormone (MIH), crustacean hyperglycemic hormone (CHH), and ion-transport peptide (ITP). Both crabs expressed a diversity of growth-related factors, such as mTOR, AKT, Rheb and AMPKα, and stress-responsive factors, including multiple heat shock proteins (HSPs). Temperature effects on the expression of key regulatory genes were quantified by qPCR in adult red king crab males kept at 4 °C or 10 °C for two weeks during intermolt. The Halloween genes tended to be upregulated in YO at high temperature, while the ecdysteroid receptor and several growth regulators showed tissue-specific responses to elevated temperature. Constitutive and heat-inducible HSPs were expressed in an inverse temperature-dependent manner, suggesting that adult red king crabs can acclimate to increased water temperatures.
Bombyx neuropeptide G protein-coupled receptor A14 and A15 are two functional G protein-coupled receptors for CCHamide neuropeptides
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CCHamides are newly identified insect neuropeptides, which are widely occurring in most insects. However, our knowledge about their signaling characteristics and physiological roles is still limited. Here, we cloned two full-length cDNAs encoding putative CCHamide receptors, Bombyx neuropeptide GPCR A14 (BNGR-A14) and -A15 (BNGR-A15), from the brain of B. mori larvae. Characterization of signaling indicated that Bombyx CCHamide-1 and CCHamide-2 are speciﬁc endogenous ligands for BNGR-A15 and BNGR-A14, respectively. Further functional assays combined with specific inhibitors demonstrated that upon activation by CCHamide-2, BNGR-A14 elicited significant increases in CRE-driven luciferase activity, intracellular Ca²⁺ mobilization and ERK1/2 phosphorylation in a G_q inhibitor-sensitive manner, while BNGR-A15 was activated by CCHamide-1, thus leading to intracellular accumulation of cAMP, Ca²⁺ mobilization, and ERK1/2 phosphorylation in a G_s and G_q inhibitor-sensitive manner. Based on these findings, we designated the receptors BNGR-A15 and -A14 as Bommo-CCHaR-1 and -2, respectively. In addition, our results showed that CCHamides are considered to require intrachain disulﬁde bonds to activate their respective receptor in the physiological concentration range. Moreover, quantitative RT-PCR analysis revealed that CCHamide-1 is more likely to serve as a brain-gut peptide to regulate feeding behavior and growth through BNGR-A15, whereas the CCHamide-2 signaling system might play an important role in the control of multiple physiological processes. Our findings provide in-depth information on CCHamide-1 and -2-mediated signaling, facilitating further elucidation of their endocrinological roles in the regulation of fundamental physiological processes.
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Two additional conserved cysteine residues are found in the invertebrate IL-17 proteins (e.g., molluscan IL-17), which potentially result in the formation of 3 disulfide bridges (Huang et al., 2015). Crustacean CFSHs exhibit 8 conserved cysteine residues, predicted to form 4 disulfide bridges (Zmora and Chung, 2014; Ventura et al., 2014; Veenstra, 2015; Veenstra, 2016; Nguyen et al., 2016; Toullec et al., 2017; Kotaka and Ohira, 2018; Tsutsui et al., 2018). However, within the IL-17 family domain region (see Fig. 4), six positions of cysteine residues are conserved among crustacean CFSHs and invertebrate IL-17 proteins, which is an important characteristic of both CFSH and IL-17.
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The southern rock lobster, Jasus edwardsii, is a member of the Achelata native to New Zealand and southern Australia that in addition to being the subject of an extensive wild fishery, has been proposed as a target for aquaculture. One obstacle to the farming of this species is its long maturation period, and the development of large-scale commercial aquaculture will require management strategies that reduce the duration of its time in culture. Increasing food intake can result in increased growth rates, and may be one way to reduce the time to market for farmed lobsters. In crustaceans, food intake and growth are regulated by locally released and/or circulating paracrines/hormones, the largest class being peptides. In the study presented here, the native peptides of J. edwardsii, as well as their cognate receptors, were predicted using a publicly accessible transcriptome. Two hundred and seventy distinct peptides were identified (the largest peptidome currently extant for any decapod), 122 of which possess structures that place them into generally recognized arthropod peptide families, i.e., adipokinetic hormone-corazonin-like peptide, allatostatin A, allatostatin B, allatostatin C, bursicon, CCHamide, corazonin, crustacean cardioactive peptide, crustacean hyperglycemic hormone/molt-inhibiting hormone, diuretic hormone 31, diuretic hormone 44, eclosion hormone, elevenin, FMRFamide-like peptide, glycoprotein hormone, GSEFLamide, inotocin, insulin-like peptide, leucokinin, myosuppressin, neuroparsin, neuropeptide F, orcokinin, orcomyotropin, pigment dispersing hormone, proctolin, pyrokinin, red pigment concentrating hormone, RYamide, short neuropeptide F, SIFamide, sulfakinin, tachykinin-related peptide and trissin. Putative receptors for many of the identified peptide groups were also identified via transcriptome mining. This is the first report of a peptidome and peptide receptors for J. edwardsii, and as such, provides a powerful new resource for beginning to investigate the physiological/behavioral roles played by peptidergic signaling systems in this species, including the roles they play in controlling processes that are of importance for improving aquaculture management strategies.
Peptidergic signaling in the tadpole shrimp Triops newberryi: A potential model for investigating the roles played by peptide paracrines/hormones in adaptation to environmental change
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Given their long history of use for investigating peptidergic signaling, it should come as no surprise that considerable effort has been directed at identifying native crustacean peptides (e.g., Christie et al., 2010a). This said, most species for which large peptidomes have been described are from the class Malacostraca, in particular members of the Decapoda, a relatively derived taxon (e.g., Bao et al., 2015; Christie, 2014a, 2014b, 2016a, 2016b, 2017; Christie and Chi, 2015a; Christie and Pascual, 2016; Christie et al., 2015, 2017a; Fu et al., 2005a, 2005b; Hui et al., 2012, 2013; Huybrechts et al., 2003; Li et al., 2003; Ma et al., 2008, 2009a, 2009b, 2010; Suwansa-Ard et al., 2015; Toullec et al., 2013, 2017; Veenstra, 2015, 2016; Ventura et al., 2014; Ye et al., 2015; Xu et al., 2015). Comparatively few large-scale peptidomic studies have been conducted on more primitive crustaceans (e.g., Christie, 2014c, 2014d, 2014e, 2014f, 2015a; Christie et al., 2011a, 2013, 2016; Dircksen et al., 2011; Gard et al., 2009; Yan et al., 2012).
Peptides are the largest/most diverse class of molecules used by animals for chemical communication, and with their cognate receptors, are key players in modulating physiological/behavioral control systems, including those involved in adaptation to environmental change. Crustaceans have long served as models for investigating peptidergic control of physiology/behavior, and members of Notostraca, an ancient branchiopod order, have recently been proposed as models for investigating the genetic/physiological underpinnings of ecoresponsiveness; nothing is currently known about the genes/proteins underlying peptidergic signaling in any member of this crustacean taxon. Transcriptome mining is a powerful tool for peptidome prediction in crustaceans, and all large-scale discovery of crustacean peptide receptors has been achieved via transcriptomics. Here, in silico transcriptome mining was used to elucidate the peptidergic signaling systems of the tadpole shrimp Triops newberryi, a member of Notostraca. Transcripts encoding putative precursor proteins and/or receptors for 28 peptide families were identified within the T. newberryi dataset. The deduced precursor proteins included those for allatostatin A, allatostatin B, allatostatin C, allatotropin, bursicon, CCHamide, crustacean cardioactive peptide, crustacean hyperglycemic hormone, diuretic hormone 44, ecdysis-triggering hormone, eclosion hormone, elevenin, FMRFamide-like peptide, glycoprotein hormone, GSEFLamide, inotocin, insulin-like peptide, neuroparsin, neuropeptide F, orcokinin/orcomyotropin, proctolin, pyrokinin/periviscerokinin, SIFamide, sulfakinin and tachykinin-related peptide; 117 distinct mature peptides were predicted from the collective set of deduced pre/preprohormones. Transcripts encoding putative receptors for most of the abovementioned peptide groups were also identified from the T. newberryi assembly, as were those for several families for which no precursors were found, i.e., corazonin, RYamide and short neuropeptide F. This is the first description of a peptidome and peptide receptors from any member of the Notostraca, and as such, provide a foundation for beginning to investigate the roles played by peptidergic signaling systems in T. newberryi and other notostracans, including how they may contribute to modulating organism-environment interactions.
Crustacean cardioactive peptides: Expression, localization, structure, and a possible involvement in regulation of egg-laying in the cuttlefish Sepia officinalis
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Furthermore, this neuropeptide is also involved in fertilization in L. migratoria since it increases the basal tonus and the frequency of spontaneous spermatheca contractions (da Silva and Lange, 2006). In C. maenas, the CCAP protein precursor (Fig. 1A) encodes one copy of a single neuropeptide: PFCNAFTGCamide (Chung et al., 2006), also found in many arthropods such as Drosophila melanogaster (Adams et al., 2000), Manduca sexta (Loi et al., 2001), Periplaneta americana (Honegger et al., 2002), Euphausia crystallorophias (Toullec et al., 2013), Homarus americanus (Christie et al., 2017), and Chorismus antarcticus (Toullec et al., 2017). From a structural point of view, analysis of the S. officinalis precursor predicted the release of 3 neuropeptides with very similar sequences, subsequently characterized by mass spectrometry (Zatylny-Gaudin et al., 2016).
The cuttlefish (Sepia officinalis) is a cephalopod mollusk distributed on the western European coast, in the West African Ocean and in the Mediterranean Sea. On the Normandy coast (France), cuttlefish is a target species of professional fishermen, so its reproduction strategy is of particular interest in the context of stock management. Egg-laying, which is coastal, is controlled by several types of regulators among which neuropeptides. The cuttlefish neuropeptidome was recently identified by Zatylny-Gaudin et al. (2016). Among the 38 neuropeptide families identified, some were significantly overexpressed in egg-laying females as compared to mature males.
This study is focused on crustacean cardioactive peptides (CCAPs), a highly expressed neuropeptide family strongly suspected of being involved in the control of egg-laying. We investigated the functional and structural characterization and tissue mapping of CCAPs, as well as the expression patterns of their receptors. CCAPs appeared to be involved in oocyte transport through the oviduct and in mechanical secretion of capsular products. Immunocytochemistry revealed that the neuropeptides were localized throughout the central nervous system (CNS) and in the nerve endings of the glands involved in egg-capsule synthesis and secretion, i.e. the oviduct gland and the main nidamental glands. The CCAP receptor was expressed in these glands and in the subesophageal mass of the CNS. Multiple sequence alignments revealed a high level of conservation of CCAP protein precursors in Sepia officinalis and Loligo pealei, two cephalopod decapods. Primary sequences of CCAPs from the two species were fully conserved, and cryptic peptides detected in the nerve endings were also partially conserved, suggesting biological activity that remains unknown for the time being.

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Research paperCharacterization of the neuropeptidome of a Southern Ocean decapod, the Antarctic shrimp Chorismus antarcticus: Focusing on a new decapod ITP-like peptide belonging to the CHH peptide family

Highlights

Abstract

Introduction

Section snippets

Materials and methods

RNAseq assemblies

Focus on CHH peptide family

Conclusions

Acknowledgments

Gen. Comp. Endocrinol.

Gen. Comp. Endocrinol.

Gen. Comp. Endocrinol.

Gen. Comp. Endocrinol.

Gen. Comp. Endocrinol.

Gen. Comp. Endocrinol.

Insect Biochem.

Comp. Biochem. Physiol. B Biochem. Mol. Biol.

J. Mol. Biol.

Gen. Comp. Endocrinol.

Peptides

Gene

Peptides

Gen. Comp. Endocrinol.

Gen. Comp. Endocrinol.

Gen. Comp. Endocrinol.

Gen. Comp. Endocrinol.

Peptides

ProtTest: selection of best-fit models of protein evolution

Bioinformatics

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Nucleic Acids Res

Research paper
Characterization of the neuropeptidome of a Southern Ocean decapod, the Antarctic shrimp Chorismus antarcticus: Focusing on a new decapod ITP-like peptide belonging to the CHH peptide family