Genome skimming reveals a multipartite mitochondrial genome in the parasitic nematode Dioctophyme renale

Autores
Baricalla, Agustin Ariel; Macchiaroli, Natalia; Fernandez Shanahan, Tomas; Ingravidi, Marina Luz; Sananez, Inés; Arce, Lucas Federico; Franchini, Gisela Raquel; Kamenetzky, Laura
Año de publicación
2025
Idioma
inglés
Tipo de recurso
artículo
Estado
versión publicada
Descripción
Background Dioctophyme renale, known as the “giant kidney worm,” is a parasitic nematode of significant medical and biological importance due to its large size and complex interactions with various mammals, including humans, causing dioctophymiasis. Despite its importance, genomic information for D. renale is limited. Only partial sequences of mitochondrial genes and 18S rRNA have been reported, classifying it within Clade I nematodes, alongside Trichuris and Trichinella. Mitochondrial genomes are valuable for phylogenetic, biogeographic, and population studies. The nematode mitochondrial genome is typically circular, encoding 12 protein-coding genes, 22 tRNAs, and two rRNAs, although some species exhibit multipartite mitogenomes. Given the lack of comprehensive genomic data, this study aims to sequence the mitogenome of D. renale using genome skimming and long-read sequencing, and to perform comparative analyses to assess its structure, composition, and phylogenetic relationships within Clade I nematodes, considering the influence of its unique life history traits. Results We found that the single circular mitochondrial chromosome typically found in animals has evolved into a multipartite organization in Dioctophyme renale, consisting of eleven minichromosomes, each containing a single protein-coding gene and an associated non-coding region. While multipartite mitogenomes have been reported in other metazoan lineages, this architecture, strongly supported by long-read sequencing from independent library constructions, represents a novel mitogenome structure within nematodes. Comparative analyses indicate that mitochondrial protein-coding sequences in D. renale cluster phylogenetically with those of vertebrate-parasitic nematodes within Clade I, whereas the structural fragmentation of the mitogenome appears to have evolved independently. Conclusions Although the functional implications of a multipartite mitogenome remain unknown, future work should examine whether specific life-history traits or selective pressures associated with parasitism may have contributed to its emergence. We also present a long-read genome-skimming workflow suitable for non-model organisms, offering a strategy to expand mitogenomic resources in taxonomic groups that remain markedly underrepresented.
Fil: Baricalla, Agustin Ariel. Universidad Nacional de San Luis; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - San Luis; Argentina
Fil: Macchiaroli, Natalia. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Instituto de Biociencias, Biotecnología y Biología Traslacional.; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - San Luis; Argentina
Fil: Fernandez Shanahan, Tomas. Universidad de Buenos Aires; Argentina
Fil: Ingravidi, Marina Luz. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Instituto de Biociencias, Biotecnología y Biología Traslacional.; Argentina
Fil: Sananez, Inés. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Instituto de Biociencias, Biotecnología y Biología Traslacional.; Argentina
Fil: Arce, Lucas Federico. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - La Plata. Instituto de Investigaciones Bioquímicas de La Plata "Prof. Dr. Rodolfo R. Brenner". Universidad Nacional de la Plata. Facultad de Ciencias Médicas. Instituto de Investigaciones Bioquímicas de La Plata "Prof. Dr. Rodolfo R. Brenner"; Argentina
Fil: Franchini, Gisela Raquel. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - La Plata. Instituto de Investigaciones Bioquímicas de La Plata "Prof. Dr. Rodolfo R. Brenner". Universidad Nacional de la Plata. Facultad de Ciencias Médicas. Instituto de Investigaciones Bioquímicas de La Plata "Prof. Dr. Rodolfo R. Brenner"; Argentina
Fil: Kamenetzky, Laura. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Instituto de Biociencias, Biotecnología y Biología Traslacional.; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina
Materia
DIOCTOPHYME RENALE
OXFORD NANOPORE SEQUENCING
PARASITE NEMATODE GENOMICS
MITOCHONDRIAL MINICHROMOSOMES
MITOGENOME FRAGMENTATION
Nivel de accesibilidad
acceso abierto
Condiciones de uso
https://creativecommons.org/licenses/by-nc-sa/2.5/ar/
Repositorio
CONICET Digital (CONICET)
Institución
Consejo Nacional de Investigaciones Científicas y Técnicas
OAI Identificador
oai:ri.conicet.gov.ar:11336/290801
Acceder
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oai_identifier_str oai:ri.conicet.gov.ar:11336/290801
network_acronym_str CONICETDig
repository_id_str 3498
network_name_str CONICET Digital (CONICET)
spelling Genome skimming reveals a multipartite mitochondrial genome in the parasitic nematode Dioctophyme renaleBaricalla, Agustin ArielMacchiaroli, NataliaFernandez Shanahan, TomasIngravidi, Marina LuzSananez, InésArce, Lucas FedericoFranchini, Gisela RaquelKamenetzky, LauraDIOCTOPHYME RENALEOXFORD NANOPORE SEQUENCINGPARASITE NEMATODE GENOMICSMITOCHONDRIAL MINICHROMOSOMESMITOGENOME FRAGMENTATIONhttps://purl.org/becyt/ford/1.2https://purl.org/becyt/ford/1https://purl.org/becyt/ford/3.3https://purl.org/becyt/ford/3https://purl.org/becyt/ford/1.6https://purl.org/becyt/ford/1Background Dioctophyme renale, known as the “giant kidney worm,” is a parasitic nematode of significant medical and biological importance due to its large size and complex interactions with various mammals, including humans, causing dioctophymiasis. Despite its importance, genomic information for D. renale is limited. Only partial sequences of mitochondrial genes and 18S rRNA have been reported, classifying it within Clade I nematodes, alongside Trichuris and Trichinella. Mitochondrial genomes are valuable for phylogenetic, biogeographic, and population studies. The nematode mitochondrial genome is typically circular, encoding 12 protein-coding genes, 22 tRNAs, and two rRNAs, although some species exhibit multipartite mitogenomes. Given the lack of comprehensive genomic data, this study aims to sequence the mitogenome of D. renale using genome skimming and long-read sequencing, and to perform comparative analyses to assess its structure, composition, and phylogenetic relationships within Clade I nematodes, considering the influence of its unique life history traits. Results We found that the single circular mitochondrial chromosome typically found in animals has evolved into a multipartite organization in Dioctophyme renale, consisting of eleven minichromosomes, each containing a single protein-coding gene and an associated non-coding region. While multipartite mitogenomes have been reported in other metazoan lineages, this architecture, strongly supported by long-read sequencing from independent library constructions, represents a novel mitogenome structure within nematodes. Comparative analyses indicate that mitochondrial protein-coding sequences in D. renale cluster phylogenetically with those of vertebrate-parasitic nematodes within Clade I, whereas the structural fragmentation of the mitogenome appears to have evolved independently. Conclusions Although the functional implications of a multipartite mitogenome remain unknown, future work should examine whether specific life-history traits or selective pressures associated with parasitism may have contributed to its emergence. We also present a long-read genome-skimming workflow suitable for non-model organisms, offering a strategy to expand mitogenomic resources in taxonomic groups that remain markedly underrepresented.Fil: Baricalla, Agustin Ariel. Universidad Nacional de San Luis; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - San Luis; ArgentinaFil: Macchiaroli, Natalia. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Instituto de Biociencias, Biotecnología y Biología Traslacional.; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - San Luis; ArgentinaFil: Fernandez Shanahan, Tomas. Universidad de Buenos Aires; ArgentinaFil: Ingravidi, Marina Luz. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Instituto de Biociencias, Biotecnología y Biología Traslacional.; ArgentinaFil: Sananez, Inés. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Instituto de Biociencias, Biotecnología y Biología Traslacional.; ArgentinaFil: Arce, Lucas Federico. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - La Plata. Instituto de Investigaciones Bioquímicas de La Plata "Prof. Dr. Rodolfo R. Brenner". Universidad Nacional de la Plata. Facultad de Ciencias Médicas. Instituto de Investigaciones Bioquímicas de La Plata "Prof. Dr. Rodolfo R. Brenner"; ArgentinaFil: Franchini, Gisela Raquel. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - La Plata. Instituto de Investigaciones Bioquímicas de La Plata "Prof. Dr. Rodolfo R. Brenner". Universidad Nacional de la Plata. Facultad de Ciencias Médicas. Instituto de Investigaciones Bioquímicas de La Plata "Prof. Dr. Rodolfo R. Brenner"; ArgentinaFil: Kamenetzky, Laura. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Instituto de Biociencias, Biotecnología y Biología Traslacional.; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; ArgentinaSpringer Nature2025-12info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionhttp://purl.org/coar/resource_type/c_6501info:ar-repo/semantics/articuloapplication/pdfapplication/pdfhttp://hdl.handle.net/11336/290801Baricalla, Agustin Ariel; Macchiaroli, Natalia; Fernandez Shanahan, Tomas; Ingravidi, Marina Luz; Sananez, Inés; et al.; Genome skimming reveals a multipartite mitochondrial genome in the parasitic nematode Dioctophyme renale; Springer Nature; Research Square; 12-2025; 1-152693-5015CONICET DigitalCONICETenginfo:eu-repo/semantics/altIdentifier/doi/10.21203/rs.3.rs-8148715/v1info:eu-repo/semantics/altIdentifier/url/https://www.researchsquare.com/article/rs-8148715/v1info:eu-repo/semantics/openAccesshttps://creativecommons.org/licenses/by-nc-sa/2.5/ar/reponame:CONICET Digital (CONICET)instname:Consejo Nacional de Investigaciones Científicas y Técnicas2026-08-25T14:37:33Zoai:ri.conicet.gov.ar:11336/290801instacron:CONICETInstitucionalhttp://ri.conicet.gov.ar/Organismo científico-tecnológicoNo correspondehttp://ri.conicet.gov.ar/oai/requestdasensio@conicet.gov.ar; lcarlino@conicet.gov.arArgentinaNo correspondeNo correspondeNo correspondeopendoar:34982026-08-25 14:37:34.356CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicasfalse
dc.title.none.fl_str_mv Genome skimming reveals a multipartite mitochondrial genome in the parasitic nematode Dioctophyme renale
title Genome skimming reveals a multipartite mitochondrial genome in the parasitic nematode Dioctophyme renale
spellingShingle Genome skimming reveals a multipartite mitochondrial genome in the parasitic nematode Dioctophyme renale
Baricalla, Agustin Ariel
DIOCTOPHYME RENALE
OXFORD NANOPORE SEQUENCING
PARASITE NEMATODE GENOMICS
MITOCHONDRIAL MINICHROMOSOMES
MITOGENOME FRAGMENTATION
title_short Genome skimming reveals a multipartite mitochondrial genome in the parasitic nematode Dioctophyme renale
title_full Genome skimming reveals a multipartite mitochondrial genome in the parasitic nematode Dioctophyme renale
title_fullStr Genome skimming reveals a multipartite mitochondrial genome in the parasitic nematode Dioctophyme renale
title_full_unstemmed Genome skimming reveals a multipartite mitochondrial genome in the parasitic nematode Dioctophyme renale
title_sort Genome skimming reveals a multipartite mitochondrial genome in the parasitic nematode Dioctophyme renale
dc.creator.none.fl_str_mv Baricalla, Agustin Ariel
Macchiaroli, Natalia
Fernandez Shanahan, Tomas
Ingravidi, Marina Luz
Sananez, Inés
Arce, Lucas Federico
Franchini, Gisela Raquel
Kamenetzky, Laura
author Baricalla, Agustin Ariel
author_facet Baricalla, Agustin Ariel
Macchiaroli, Natalia
Fernandez Shanahan, Tomas
Ingravidi, Marina Luz
Sananez, Inés
Arce, Lucas Federico
Franchini, Gisela Raquel
Kamenetzky, Laura
author_role author
author2 Macchiaroli, Natalia
Fernandez Shanahan, Tomas
Ingravidi, Marina Luz
Sananez, Inés
Arce, Lucas Federico
Franchini, Gisela Raquel
Kamenetzky, Laura
author2_role author
author
author
author
author
author
author
dc.subject.none.fl_str_mv DIOCTOPHYME RENALE
OXFORD NANOPORE SEQUENCING
PARASITE NEMATODE GENOMICS
MITOCHONDRIAL MINICHROMOSOMES
MITOGENOME FRAGMENTATION
topic DIOCTOPHYME RENALE
OXFORD NANOPORE SEQUENCING
PARASITE NEMATODE GENOMICS
MITOCHONDRIAL MINICHROMOSOMES
MITOGENOME FRAGMENTATION
purl_subject.fl_str_mv https://purl.org/becyt/ford/1.2
https://purl.org/becyt/ford/1
https://purl.org/becyt/ford/3.3
https://purl.org/becyt/ford/3
https://purl.org/becyt/ford/1.6
https://purl.org/becyt/ford/1
dc.description.none.fl_txt_mv Background Dioctophyme renale, known as the “giant kidney worm,” is a parasitic nematode of significant medical and biological importance due to its large size and complex interactions with various mammals, including humans, causing dioctophymiasis. Despite its importance, genomic information for D. renale is limited. Only partial sequences of mitochondrial genes and 18S rRNA have been reported, classifying it within Clade I nematodes, alongside Trichuris and Trichinella. Mitochondrial genomes are valuable for phylogenetic, biogeographic, and population studies. The nematode mitochondrial genome is typically circular, encoding 12 protein-coding genes, 22 tRNAs, and two rRNAs, although some species exhibit multipartite mitogenomes. Given the lack of comprehensive genomic data, this study aims to sequence the mitogenome of D. renale using genome skimming and long-read sequencing, and to perform comparative analyses to assess its structure, composition, and phylogenetic relationships within Clade I nematodes, considering the influence of its unique life history traits. Results We found that the single circular mitochondrial chromosome typically found in animals has evolved into a multipartite organization in Dioctophyme renale, consisting of eleven minichromosomes, each containing a single protein-coding gene and an associated non-coding region. While multipartite mitogenomes have been reported in other metazoan lineages, this architecture, strongly supported by long-read sequencing from independent library constructions, represents a novel mitogenome structure within nematodes. Comparative analyses indicate that mitochondrial protein-coding sequences in D. renale cluster phylogenetically with those of vertebrate-parasitic nematodes within Clade I, whereas the structural fragmentation of the mitogenome appears to have evolved independently. Conclusions Although the functional implications of a multipartite mitogenome remain unknown, future work should examine whether specific life-history traits or selective pressures associated with parasitism may have contributed to its emergence. We also present a long-read genome-skimming workflow suitable for non-model organisms, offering a strategy to expand mitogenomic resources in taxonomic groups that remain markedly underrepresented.
Fil: Baricalla, Agustin Ariel. Universidad Nacional de San Luis; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - San Luis; Argentina
Fil: Macchiaroli, Natalia. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Instituto de Biociencias, Biotecnología y Biología Traslacional.; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - San Luis; Argentina
Fil: Fernandez Shanahan, Tomas. Universidad de Buenos Aires; Argentina
Fil: Ingravidi, Marina Luz. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Instituto de Biociencias, Biotecnología y Biología Traslacional.; Argentina
Fil: Sananez, Inés. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Instituto de Biociencias, Biotecnología y Biología Traslacional.; Argentina
Fil: Arce, Lucas Federico. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - La Plata. Instituto de Investigaciones Bioquímicas de La Plata "Prof. Dr. Rodolfo R. Brenner". Universidad Nacional de la Plata. Facultad de Ciencias Médicas. Instituto de Investigaciones Bioquímicas de La Plata "Prof. Dr. Rodolfo R. Brenner"; Argentina
Fil: Franchini, Gisela Raquel. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - La Plata. Instituto de Investigaciones Bioquímicas de La Plata "Prof. Dr. Rodolfo R. Brenner". Universidad Nacional de la Plata. Facultad de Ciencias Médicas. Instituto de Investigaciones Bioquímicas de La Plata "Prof. Dr. Rodolfo R. Brenner"; Argentina
Fil: Kamenetzky, Laura. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Instituto de Biociencias, Biotecnología y Biología Traslacional.; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina
description Background Dioctophyme renale, known as the “giant kidney worm,” is a parasitic nematode of significant medical and biological importance due to its large size and complex interactions with various mammals, including humans, causing dioctophymiasis. Despite its importance, genomic information for D. renale is limited. Only partial sequences of mitochondrial genes and 18S rRNA have been reported, classifying it within Clade I nematodes, alongside Trichuris and Trichinella. Mitochondrial genomes are valuable for phylogenetic, biogeographic, and population studies. The nematode mitochondrial genome is typically circular, encoding 12 protein-coding genes, 22 tRNAs, and two rRNAs, although some species exhibit multipartite mitogenomes. Given the lack of comprehensive genomic data, this study aims to sequence the mitogenome of D. renale using genome skimming and long-read sequencing, and to perform comparative analyses to assess its structure, composition, and phylogenetic relationships within Clade I nematodes, considering the influence of its unique life history traits. Results We found that the single circular mitochondrial chromosome typically found in animals has evolved into a multipartite organization in Dioctophyme renale, consisting of eleven minichromosomes, each containing a single protein-coding gene and an associated non-coding region. While multipartite mitogenomes have been reported in other metazoan lineages, this architecture, strongly supported by long-read sequencing from independent library constructions, represents a novel mitogenome structure within nematodes. Comparative analyses indicate that mitochondrial protein-coding sequences in D. renale cluster phylogenetically with those of vertebrate-parasitic nematodes within Clade I, whereas the structural fragmentation of the mitogenome appears to have evolved independently. Conclusions Although the functional implications of a multipartite mitogenome remain unknown, future work should examine whether specific life-history traits or selective pressures associated with parasitism may have contributed to its emergence. We also present a long-read genome-skimming workflow suitable for non-model organisms, offering a strategy to expand mitogenomic resources in taxonomic groups that remain markedly underrepresented.
publishDate 2025
dc.date.none.fl_str_mv 2025-12
dc.type.none.fl_str_mv info:eu-repo/semantics/article
info:eu-repo/semantics/publishedVersion
http://purl.org/coar/resource_type/c_6501
info:ar-repo/semantics/articulo
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/11336/290801
Baricalla, Agustin Ariel; Macchiaroli, Natalia; Fernandez Shanahan, Tomas; Ingravidi, Marina Luz; Sananez, Inés; et al.; Genome skimming reveals a multipartite mitochondrial genome in the parasitic nematode Dioctophyme renale; Springer Nature; Research Square; 12-2025; 1-15
2693-5015
CONICET Digital
CONICET
url http://hdl.handle.net/11336/290801
identifier_str_mv Baricalla, Agustin Ariel; Macchiaroli, Natalia; Fernandez Shanahan, Tomas; Ingravidi, Marina Luz; Sananez, Inés; et al.; Genome skimming reveals a multipartite mitochondrial genome in the parasitic nematode Dioctophyme renale; Springer Nature; Research Square; 12-2025; 1-15
2693-5015
CONICET Digital
CONICET
dc.language.none.fl_str_mv eng
language eng
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info:eu-repo/semantics/altIdentifier/url/https://www.researchsquare.com/article/rs-8148715/v1
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
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eu_rights_str_mv openAccess
rights_invalid_str_mv https://creativecommons.org/licenses/by-nc-sa/2.5/ar/
dc.format.none.fl_str_mv application/pdf
application/pdf
dc.publisher.none.fl_str_mv Springer Nature
publisher.none.fl_str_mv Springer Nature
dc.source.none.fl_str_mv reponame:CONICET Digital (CONICET)
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repository.mail.fl_str_mv dasensio@conicet.gov.ar; lcarlino@conicet.gov.ar
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