Cargando…

An insight into the functional genomics and species classification of Eudiplozoon nipponicum (Monogenea, Diplozoidae), a haematophagous parasite of the common carp Cyprinus carpio

BACKGROUND: Monogenea (Platyhelminthes, Neodermata) are the most species-rich class within the Neodermata superclass of primarily fish parasites. Despite their economic and ecological importance, monogenean research tends to focus on their morphological, phylogenetic, and population characteristics,...

Descripción completa

Detalles Bibliográficos
Autores principales: Vorel, Jiří, Kmentová, Nikol, Hahn, Christoph, Bureš, Petr, Kašný, Martin
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10308649/
https://www.ncbi.nlm.nih.gov/pubmed/37380941
http://dx.doi.org/10.1186/s12864-023-09461-8
_version_ 1785066289712070656
author Vorel, Jiří
Kmentová, Nikol
Hahn, Christoph
Bureš, Petr
Kašný, Martin
author_facet Vorel, Jiří
Kmentová, Nikol
Hahn, Christoph
Bureš, Petr
Kašný, Martin
author_sort Vorel, Jiří
collection PubMed
description BACKGROUND: Monogenea (Platyhelminthes, Neodermata) are the most species-rich class within the Neodermata superclass of primarily fish parasites. Despite their economic and ecological importance, monogenean research tends to focus on their morphological, phylogenetic, and population characteristics, while comprehensive omics analyses aimed at describing functionally important molecules are few and far between. We present a molecular characterisation of monogenean representative Eudiplozoon nipponicum, an obligate haematophagous parasite infecting the gills of the common carp. We report its nuclear and mitochondrial genomes, present a functional annotation of protein molecules relevant to the molecular and biochemical aspect of physiological processes involved in interactions with the fish hosts, and re-examinate the taxonomic position of Eudiplozoon species within the Diplozoidae family. RESULTS: We have generated 50.81 Gbp of raw sequencing data (Illumina and Oxford Nanopore reads), bioinformatically processed, and de novo assembled them into a genome draft 0.94 Gbp long, consisting of 21,044 contigs (N50 = 87 kbp). The final assembly represents 57% of the estimated total genome size (~ 1.64 Gbp), whereby repetitive and low-complexity regions account for ~ 64% of the assembled length. In total, 36,626 predicted genes encode 33,031 proteins and homology-based annotation of protein-coding genes (PCGs) and proteins characterises 14,785 (44.76%) molecules. We have detected significant representation of functional proteins and known molecular functions. The numbers of peptidases and inhibitors (579 proteins), characterised GO terms (16,016 unique assigned GO terms), and identified KEGG Orthology (4,315 proteins) acting in 378 KEGG pathways demonstrate the variety of mechanisms by which the parasite interacts with hosts on a macromolecular level (immunomodulation, feeding, and development). Comparison between the newly assembled E. nipponicum mitochondrial genome (length of 17,038 bp) and other diplozoid monogeneans confirms the existence of two distinct Eudiplozoon species infecting different fish hosts: Cyprinus carpio and Carassius spp. CONCLUSIONS: Although the amount of sequencing data and characterised molecules of monogenean parasites has recently increased, a better insight into their molecular biology is needed. The E. nipponicum nuclear genome presented here, currently the largest described genome of any monogenean parasite, represents a milestone in the study of monogeneans and their molecules but further omics research is needed to understand these parasites’ biological nature. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12864-023-09461-8.
format Online
Article
Text
id pubmed-10308649
institution National Center for Biotechnology Information
language English
publishDate 2023
publisher BioMed Central
record_format MEDLINE/PubMed
spelling pubmed-103086492023-06-30 An insight into the functional genomics and species classification of Eudiplozoon nipponicum (Monogenea, Diplozoidae), a haematophagous parasite of the common carp Cyprinus carpio Vorel, Jiří Kmentová, Nikol Hahn, Christoph Bureš, Petr Kašný, Martin BMC Genomics Research BACKGROUND: Monogenea (Platyhelminthes, Neodermata) are the most species-rich class within the Neodermata superclass of primarily fish parasites. Despite their economic and ecological importance, monogenean research tends to focus on their morphological, phylogenetic, and population characteristics, while comprehensive omics analyses aimed at describing functionally important molecules are few and far between. We present a molecular characterisation of monogenean representative Eudiplozoon nipponicum, an obligate haematophagous parasite infecting the gills of the common carp. We report its nuclear and mitochondrial genomes, present a functional annotation of protein molecules relevant to the molecular and biochemical aspect of physiological processes involved in interactions with the fish hosts, and re-examinate the taxonomic position of Eudiplozoon species within the Diplozoidae family. RESULTS: We have generated 50.81 Gbp of raw sequencing data (Illumina and Oxford Nanopore reads), bioinformatically processed, and de novo assembled them into a genome draft 0.94 Gbp long, consisting of 21,044 contigs (N50 = 87 kbp). The final assembly represents 57% of the estimated total genome size (~ 1.64 Gbp), whereby repetitive and low-complexity regions account for ~ 64% of the assembled length. In total, 36,626 predicted genes encode 33,031 proteins and homology-based annotation of protein-coding genes (PCGs) and proteins characterises 14,785 (44.76%) molecules. We have detected significant representation of functional proteins and known molecular functions. The numbers of peptidases and inhibitors (579 proteins), characterised GO terms (16,016 unique assigned GO terms), and identified KEGG Orthology (4,315 proteins) acting in 378 KEGG pathways demonstrate the variety of mechanisms by which the parasite interacts with hosts on a macromolecular level (immunomodulation, feeding, and development). Comparison between the newly assembled E. nipponicum mitochondrial genome (length of 17,038 bp) and other diplozoid monogeneans confirms the existence of two distinct Eudiplozoon species infecting different fish hosts: Cyprinus carpio and Carassius spp. CONCLUSIONS: Although the amount of sequencing data and characterised molecules of monogenean parasites has recently increased, a better insight into their molecular biology is needed. The E. nipponicum nuclear genome presented here, currently the largest described genome of any monogenean parasite, represents a milestone in the study of monogeneans and their molecules but further omics research is needed to understand these parasites’ biological nature. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12864-023-09461-8. BioMed Central 2023-06-29 /pmc/articles/PMC10308649/ /pubmed/37380941 http://dx.doi.org/10.1186/s12864-023-09461-8 Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Vorel, Jiří
Kmentová, Nikol
Hahn, Christoph
Bureš, Petr
Kašný, Martin
An insight into the functional genomics and species classification of Eudiplozoon nipponicum (Monogenea, Diplozoidae), a haematophagous parasite of the common carp Cyprinus carpio
title An insight into the functional genomics and species classification of Eudiplozoon nipponicum (Monogenea, Diplozoidae), a haematophagous parasite of the common carp Cyprinus carpio
title_full An insight into the functional genomics and species classification of Eudiplozoon nipponicum (Monogenea, Diplozoidae), a haematophagous parasite of the common carp Cyprinus carpio
title_fullStr An insight into the functional genomics and species classification of Eudiplozoon nipponicum (Monogenea, Diplozoidae), a haematophagous parasite of the common carp Cyprinus carpio
title_full_unstemmed An insight into the functional genomics and species classification of Eudiplozoon nipponicum (Monogenea, Diplozoidae), a haematophagous parasite of the common carp Cyprinus carpio
title_short An insight into the functional genomics and species classification of Eudiplozoon nipponicum (Monogenea, Diplozoidae), a haematophagous parasite of the common carp Cyprinus carpio
title_sort insight into the functional genomics and species classification of eudiplozoon nipponicum (monogenea, diplozoidae), a haematophagous parasite of the common carp cyprinus carpio
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10308649/
https://www.ncbi.nlm.nih.gov/pubmed/37380941
http://dx.doi.org/10.1186/s12864-023-09461-8
work_keys_str_mv AT voreljiri aninsightintothefunctionalgenomicsandspeciesclassificationofeudiplozoonnipponicummonogeneadiplozoidaeahaematophagousparasiteofthecommoncarpcyprinuscarpio
AT kmentovanikol aninsightintothefunctionalgenomicsandspeciesclassificationofeudiplozoonnipponicummonogeneadiplozoidaeahaematophagousparasiteofthecommoncarpcyprinuscarpio
AT hahnchristoph aninsightintothefunctionalgenomicsandspeciesclassificationofeudiplozoonnipponicummonogeneadiplozoidaeahaematophagousparasiteofthecommoncarpcyprinuscarpio
AT burespetr aninsightintothefunctionalgenomicsandspeciesclassificationofeudiplozoonnipponicummonogeneadiplozoidaeahaematophagousparasiteofthecommoncarpcyprinuscarpio
AT kasnymartin aninsightintothefunctionalgenomicsandspeciesclassificationofeudiplozoonnipponicummonogeneadiplozoidaeahaematophagousparasiteofthecommoncarpcyprinuscarpio
AT voreljiri insightintothefunctionalgenomicsandspeciesclassificationofeudiplozoonnipponicummonogeneadiplozoidaeahaematophagousparasiteofthecommoncarpcyprinuscarpio
AT kmentovanikol insightintothefunctionalgenomicsandspeciesclassificationofeudiplozoonnipponicummonogeneadiplozoidaeahaematophagousparasiteofthecommoncarpcyprinuscarpio
AT hahnchristoph insightintothefunctionalgenomicsandspeciesclassificationofeudiplozoonnipponicummonogeneadiplozoidaeahaematophagousparasiteofthecommoncarpcyprinuscarpio
AT burespetr insightintothefunctionalgenomicsandspeciesclassificationofeudiplozoonnipponicummonogeneadiplozoidaeahaematophagousparasiteofthecommoncarpcyprinuscarpio
AT kasnymartin insightintothefunctionalgenomicsandspeciesclassificationofeudiplozoonnipponicummonogeneadiplozoidaeahaematophagousparasiteofthecommoncarpcyprinuscarpio