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Trematode DIPLOSTOMUM PSEUDOSPATHACEUM INDUCING DIFFERENTIAL GENE EXPRESSION IN SEXUAL AND GYNOGENETIC GIBEL CARP (Carassius gibelio): PARASITES FACILITATING THE COEXISTENCE OF TWO REPRODUCTIVE FORMS of the invasive species

ABSTRACT: Trematode DIPLOSTOMUM PSEUDOSPATHACEUM INDUCING DIFFERENTIAL GENE EXPRESSION IN SEXUAL AND GYNOGENETIC GIBEL CARP (Carassius gibelio): PARASITES FACILITATING THE COEXISTENCE OF TWO REPRODUCTIVE FORMS of the invasive species

PROVIDER: PRJNA1077946 | ENA |

REPOSITORIES: ENA

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			Action	DRS
	SRR28006337_1.fastq.gz	Fastqsanger.gz
	SRR28006337_2.fastq.gz	Fastqsanger.gz
	SRR28006338_1.fastq.gz	Fastqsanger.gz
	SRR28006338_2.fastq.gz	Fastqsanger.gz
	SRR28006339_1.fastq.gz	Fastqsanger.gz

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Project description:Parasite-mediated selection is considered one of the potential mechanisms contributing to the coexistence of asexual-sexual complexes. Gibel carp (Carassius gibelio), an invasive fish species in Europe, often forms populations composed of gynogenetic and sexual specimens. In the present study, experimental infection was induced in gynogenetic and sexual gibel carp using eye-fluke Diplostomum pseudospathaceum (Trematoda), and the transcriptome profile of the spleen as a major immune organ in fish was analyzed to reveal the differentially expressed immunity-associated genes related to D. pseudospathaceum infection differing between gynogenetic and sexual gibel carp. High parasite infection was found in gynogenetic fish when compared to genetically diverse sexuals. Although metacercariae of D. pseudospathaceum are situated in an immune-privileged organ, our results show that eye trematodes may induce a host immune response. We found differential gene expression induced by eye-fluke infection, with various impacts on gynogenetic and sexual hosts, documenting for the majority of DEGs upregulation in sexuals, and downregulation in asexuals. Differences in gene regulation between gynogenetic and sexual gibel carp were evidenced in many immunity-associated genes. GO analyses revealed the importance of genes assigned to the GO terms: immune function, the Notch signaling pathway, MAP kinase tyrosine/threonine/phosphatase activity, and chemokine receptor activity. KEGG analyses revealed the importance of the genes involved in 12 immunity-associated pathways – specifically, FoxO signaling, adipocytokine signaling, TGF-beta signaling, apoptosis, Notch signaling, C-type lectin receptor signaling, efferocytosis, intestinal immune network for IgA production, insulin signaling, virion - human immunodeficiency virus, Toll-like receptor signaling, and phosphatidylinositol signaling system. Our study indicates the limited potential of asexual fish to cope with higher parasite infection (likely a loss of capacity to induce an effective immune response) and highlights the important role of molecular mechanisms associated with immunity for the coexistence of gynogenetic and sexual gibel carp, potentially contributing to its invasiveness.

Project description:Gibel carp (Carassius gibelio) is a cyprinid fish that originated in eastern Eurasia and is considered as invasive in European freshwater ecosystems. The populations of gibel carp in Europe are mostly composed of asexually reproducing triploid females (i.e., reproducing by gynogenesis) and sexually reproducing diploid females and males. Although some cases of coexisting sexual and asexual reproductive forms are known in vertebrates, the molecular mechanisms maintaining such coexistence are still in question. Both reproduction modes are supposed to exhibit evolutionary and ecological advantages and disadvantages. To better understand the coexistence of these two reproduction strategies, we performed transcriptome profile analysis of gonad tissues (ovaries), and studied the differentially expressed reproduction-associated genes in sexual and asexual females. We used high-throughput RNA sequencing to generate transcriptomic profiles of gonadal tissues of triploid asexual females and males, diploid sexual males and females of gibel carp, as well as diploid individuals from two closely-related species, C. auratus and Cyprinus carpio. Using SNP clustering, we showed the close similarity of C. gibelio and C. auratus with a basal position of C. carpio to both Carassius species. Using transcriptome profile analyses, we showed that many genes and pathways are involved in both gynogenetic and sexual reproduction in C. gibelio; however, we also found that 1500 genes, including 100 genes involved in cell cycle control, meiosis, oogenesis, embryogenesis, fertilization, steroid hormone signaling and biosynthesis were differently expressed in the ovaries of asexual and sexual females. We suggest that the overall downregulation of reproduction-associated pathways in asexual females, and their maintenance in sexual ones, allow for their stable coexistence, integrating the evolutionary and ecological advantages and disadvantages of the two reproductive forms. However, we showed that many sexual-reproduction-related genes are maintained and expressed in asexual females, suggesting that gynogenetic gibel carp retains the genetic toolkits for meiosis and sexual reproduction. These findings shed new light on the evolution of this asexual and sexual complex.

Project description:Sex in vertebrates is commonly determined by genotype and in some cases by environmental conditions, such as temperature. A few vertebrate species display intermediate conditions of sex determination, combining sex chromosomes with an effect of temperature. This phenomenon is known for the gibel carp (Carassius gibelio), an invasive cyprinid fish species, whose abilities to adapt and colonize new environments is linked with the combination of sexual and asexual reproduction. In this study, the gonad transcriptomes were compared between genotypic males and temperature-induced males of C. gibelio. We specifically focused on the meiosis-related and reproduction-associated genes. Many genes and pathways of cell cycle control and meiosis, male differentiation and spermatogenesis were common to genotypic and temperature-induced males of gibel carp. However, the underrepresentation of several GO terms and KEGG pathways related to reproduction and spermatogenesis in genotypic males suggests lower reproductive abilities of temperature-induced males. Our study highlights the differential transcription regulation of key genes related to male sex differentiation, steroid hormone regulation, meiosis, spermatogenesis and sperm-egg interaction including the genes associated with sperm fertilization, motility and sperm flagellum function. Especially, induced males strongly overexpressed hsd17b2 and slightly overexpressed the meiotic gene mnd1, while genotypic males overexpressed sox8a and cyp19a1a, as well as the crucial fertilization gene izumo. These findings contribute to the understanding of the molecular mechanisms underlying the reproductive plasticity and invasiveness of C. gibelio in Europe. Our study highlighs the role of males, whose appearance was crucial for the transition from asexual to sexual reproduction in this species. Our findings contribute to the understanding of the molecular mechanisms underlying the reproductive plasticity and invasiveness of C. gibelio in Europe.

Project description:IntroductionParasite-mediated selection is considered one of the potential mechanisms contributing to the coexistence of asexual-sexual complexes. Gibel carp (Carassius gibelio), an invasive fish species in Europe, often forms populations composed of gynogenetic and sexual specimens.MethodsThe experimental infection was induced in gynogenetic and sexual gibel carp using eye-fluke Diplostomum pseudospathaceum (Trematoda), and the transcriptome profile of the spleen as a major immune organ in fish was analyzed to reveal the differentially expressed immunity-associated genes related to D. pseudospathaceum infection differing between gynogenetic and sexual gibel carp.ResultsHigh parasite infection was found in gynogenetic fish when compared to genetically diverse sexuals. Although metacercariae of D. pseudospathaceum are situated in an immune-privileged organ, our results show that eye trematodes may induce a host immune response. We found differential gene expression induced by eye-fluke infection, with various impacts on gynogenetic and sexual hosts, documenting for the majority of DEGs upregulation in sexuals, and downregulation in asexuals. Differences in gene regulation between gynogenetic and sexual gibel carp were evidenced in many immunity-associated genes. GO analyses revealed the importance of genes assigned to the GO terms: immune function, the Notch signaling pathway, MAP kinase tyrosine/threonine/phosphatase activity, and chemokine receptor activity. KEGG analyses revealed the importance of the genes involved in 12 immunity-associated pathways - specifically, FoxO signaling, adipocytokine signaling, TGF-beta signaling, apoptosis, Notch signaling, C-type lectin receptor signaling, efferocytosis, intestinal immune network for IgA production, insulin signaling, virion - human immunodeficiency virus, Toll-like receptor signaling, and phosphatidylinositol signaling system.DiscussionOur study indicates the limited potential of asexual fish to cope with higher parasite infection (likely a loss of capacity to induce an effective immune response) and highlights the important role of molecular mechanisms associated with immunity for the coexistence of gynogenetic and sexual gibel carp, potentially contributing to its invasiveness.

Dataset Information

Trematode DIPLOSTOMUM PSEUDOSPATHACEUM INDUCING DIFFERENTIAL GENE EXPRESSION IN SEXUAL AND GYNOGENETIC GIBEL CARP (Carassius gibelio): PARASITES FACILITATING THE COEXISTENCE OF TWO REPRODUCTIVE FORMS of the invasive species

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