Premetazoan Origin of Neuropeptide Signaling

Molecular Biology and Evolution, Journal Year: 2022, Volume and Issue: 39(4)

Published: March 7, 2022

Abstract Neuropeptides are a diverse class of signaling molecules in metazoans. They occur all animals with nervous system and also neuron-less placozoans. However, their origin has remained unclear because no neuropeptide shows deep homology across lineages, none have been found sponges. Here, we identify two precursors, phoenixin (PNX) nesfatin, broad evolutionary conservation. By database searches, sequence alignments, gene-structure comparisons, show that both precursors present bilaterians, cnidarians, ctenophores, We PNX secreted nesfatin precursor homolog the choanoflagellate Salpingoeca rosetta. PNX, particular, is highly conserved, including its cleavage sites, suggesting prohormone processing occurs choanoflagellates. In addition, based on phyletic patterns negative pharmacological assays, question originally proposed GPR-173 (SREB3) as receptor. Our findings revealed homologs derived from longer premetazoan origins thus evolved before neurons.

Language: Английский

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Cholecystokinin/sulfakinin peptide signaling: conserved roles at the intersection between feeding, mating and aggression

Cellular and Molecular Life Sciences, Journal Year: 2022, Volume and Issue: 79(3)

Published: March 1, 2022

Neuropeptides are the most diverse messenger molecules in metazoans and involved regulation of daily physiology a wide array behaviors. Some neuropeptides their cognate receptors structurally functionally well conserved over evolution bilaterian animals. Among these peptides related to gastrin cholecystokinin (CCK). In mammals, CCK is produced by intestinal endocrine cells brain neurons, regulates gall bladder contractions, pancreatic enzyme secretion, gut functions, satiety food intake. Additionally, plays important roles neuromodulation several circuits that regulate reward, anxiety, aggression sexual behavior. invertebrates, CCK-type (sulfakinins, SKs) are, with few exceptions, neurons only. Common among invertebrates SKs mediate ingestion variety mechanisms. Also secretion digestive enzymes has been reported. Studies genetically tractable fly Drosophila have advanced our understanding SK signaling mechanisms feeding, but also gustatory sensitivity, locomotor activity, reproductive A set eight SK-expressing competing males, they integrate internal state external stimuli diminish sex drive increase aggression. The same sugar gustation, induce reduce feeding. Although functional CCK/SK appear between available data suggest underlying differ.

Language: Английский

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Distinct genomic routes underlie transitions to specialised symbiotic lifestyles in deep-sea annelid worms

Nature Communications, Journal Year: 2023, Volume and Issue: 14(1)

Published: May 17, 2023

Bacterial symbioses allow annelids to colonise extreme ecological niches, such as hydrothermal vents and whale falls. Yet, the genetic principles sustaining these remain unclear. Here, we show that different genomic adaptations underpin of phylogenetically related with distinct nutritional strategies. Genome compaction extensive gene losses distinguish heterotrophic symbiosis bone-eating worm Osedax frankpressi from chemoautotrophic deep-sea Vestimentifera. Osedax's endosymbionts complement many host's metabolic deficiencies, including loss pathways recycle nitrogen synthesise some amino acids. possess glyoxylate cycle, which could more efficient catabolism bone-derived nutrients production carbohydrates fatty Unlike in most Vestimentifera, innate immunity genes are reduced O. frankpressi, which, however, has an expansion matrix metalloproteases digest collagen. Our study supports interactions influence host genome evolution differently highly specialised symbioses.

Language: Английский

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Evolutionary conserved peptide and glycoprotein hormone-like neuroendocrine systems in C. elegans

Molecular and Cellular Endocrinology, Journal Year: 2024, Volume and Issue: 584, P. 112162 - 112162

Published: Jan. 28, 2024

Peptides and protein hormones form the largest group of secreted signals that mediate intercellular communication are central regulators physiology behavior in all animals. Phylogenetic analyses biochemical identifications peptide-receptor systems reveal a broad evolutionary conservation these signaling at molecular level. Substantial progress has been made recent years on characterizing physiological putative ancestral roles many peptide through comparative studies invertebrate models. Several peptides not only molecularly conserved but also have across animal phyla. Here, we focus functional insights gained nematode Caenorhabditis elegans that, with its compact well-described nervous system, provides powerful model to dissect neuroendocrine networks involved control behavior. We summarize discoveries knowledge functions hormone C. elegans.

Language: Английский

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Spiralian genomics and the evolution of animal genome architecture

Briefings in Functional Genomics, Journal Year: 2023, Volume and Issue: 22(6), P. 498 - 508

Published: July 28, 2023

Abstract Recent developments in sequencing technologies have greatly improved our knowledge of phylogenetic relationships and genomic architectures throughout the tree life. Spiralia, a diverse clade within Protostomia, is essential for understanding evolutionary history parasitism, gene conversion, nervous systems animal body plans. In this review, we focus on current hypotheses spiralian phylogeny investigate impact long-read quality genome assemblies. We examine chromosome-level assemblies to highlight key features that driven evolution, including karyotype, synteny Hox organization. addition, show how chromosome rearrangement has influenced structures. Although genomes undergone substantial changes, they exhibit both conserved lineage-specific features. recommend increasing efforts expanding functional genomics research deepen insights into biology.

Language: Английский

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Single-cell atlases of two lophotrochozoan larvae highlight their complex evolutionary histories

Science Advances, Journal Year: 2023, Volume and Issue: 9(31)

Published: Aug. 2, 2023

Pelagic larval stages are widespread across animals, yet it is unclear whether larvae were present in the last common ancestor of animals or they evolved multiple times due to selective pressures. Many marine at least superficially similar; small, swim through beating bands cilia, and sense environment with an apical organ. To understand these similarities, we have generated single-cell atlases for from two animal phyla compared their cell types. We found clear similarities among ciliary band cells between neurons organ pointing possible homology structures, suggesting a single origin within Spiralia. also find several clade-specific innovations each larva, including distinct myocytes shell gland oyster larva. Oyster express many recently genes that made previous gene age estimates trochophore too young.

Language: Английский

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Revisiting the evolution of Family B1 GPCRs and ligands: Insights from mollusca

Molecular and Cellular Endocrinology, Journal Year: 2024, Volume and Issue: 586, P. 112192 - 112192

Published: Feb. 24, 2024

Family B1 G protein-coupled receptors (GPCRs) are one of the most well studied neuropeptide receptor families since they play a central role in many biological processes including endocrine, gastrointestinal, cardiovascular and reproduction animals. The genes for these emerged from common ancestral gene bilaterian genomes evolved via gene/genome duplications deletions vertebrate invertebrate genomes. Their existence function have mostly been characterized vertebrates few studies exist species. Recently, an increased interest molluscs, means series become available, less modified than insect nematode genomes, ideal to explore origin evolution families. This review provides overview GPCRs their peptide ligands incorporates new data obtained Mollusca taking comparative approach challenges existing models on evolution.

Language: Английский

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Somatostatin-type and allatostatin-C–type neuropeptides are paralogous and have opposing myoregulatory roles in an echinoderm

Proceedings of the National Academy of Sciences, Journal Year: 2022, Volume and Issue: 119(7)

Published: Feb. 10, 2022

Somatostatin (SS) and allatostatin-C (ASTC) are inhibitory neuropeptides in chordates protostomes, respectively, which hitherto were identified as orthologs. However, echinoderms have two SS/ASTC-type (SS1 SS2), here, our analysis of sequence data indicates that SS1 is an ortholog ASTC SS2 SS. The occurrence both SS-type ASTC-type provides a unique context to compare their physiological roles. Investigation the expression actions neuropeptide ArSS1 starfish Asterias rubens revealed it causes muscle contraction (myoexcitation), contrasting with myoinhibitory effects ArSS2. Our findings suggest paralogous originated by gene duplication common ancestor Bilateria, only one type being retained protostomes but types echinoderms. Loss may been due functional redundancy regulators processes. Conversely, retention be consequence evolution myoexcitatory role for mediated yet unknown signaling mechanisms.

Language: Английский

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Molecular and cellular architecture of the larval sensory organ in the cnidarian Nematostella vectensis

Development, Journal Year: 2022, Volume and Issue: 149(16)

Published: Aug. 15, 2022

ABSTRACT Cnidarians are the only non-bilaterian group to evolve ciliated larvae with an apical sensory organ, which is possibly homologous organs of bilaterian primary larvae. Here, we generated transcriptomes tissue in sea anemone Nematostella vectensis and showed that it has a unique neuronal signature. By integrating previously published larval single-cell data our transcriptomes, discovered domain comprises minimum six distinct cell types. We show organ compartmentalised into tuft cells (spot) larval-specific neurons (ring). Finally, identify ISX-like (NVE14554), PRD class homeobox gene specifically expressed cells, as FGF signalling-dependent transcription factor responsible for formation via repression neural ring fate cells. With this study, contribute comparison molecular anatomy organs, must be carried out across phyla determine whether crucial structure evolved once or multiple times.

Language: Английский

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Cellular‐resolution gene expression mapping reveals organization in the head ganglia of the gastropod, Berghia stephanieae

The Journal of Comparative Neurology, Journal Year: 2024, Volume and Issue: 532(6)

Published: June 1, 2024

Abstract Gastropod molluscs such as Aplysia , Lymnaea and Tritonia have been important for determining fundamental rules of motor control, learning, memory because their large, individually identifiable neurons. Yet only a small number gastropod neurons known molecular markers, limiting the ability to establish brain‐wide structure–function relations. Here we combine high‐throughput, single‐cell RNA sequencing with in situ hybridization chain reaction nudibranch Berghia stephanieae identify visualize expression markers cell types. Broad neuronal classes were characterized by genes associated neurotransmitters, like acetylcholine, glutamate, serotonin, GABA, well neuropeptides. These subdivided other including transcriptional regulators unannotated genes. Marker expressed glia formed discrete, previously unrecognized regions within between ganglia. This study provides foundation understanding cellular organization nervous systems.

Language: Английский

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