Functional insights into the infective larval stage of Anisakis simplex s.s., Anisakis pegreffii and their hybrids based on gene expression patterns
Abstract Background Anisakis simplex sensu stricto and Anisakis pegreffii are sibling species of nematodes parasitic on marine mammals. Zoonotic human infection with third stage infective larvae causes anisakiasis, a debilitating and potentially fatal disease. These 2 species show evidence of hybrid...
| Main Authors: | , , , , , , , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
BMC
2018-08-01
|
| Series: | BMC Genomics |
| Subjects: | |
| Online Access: | http://link.springer.com/article/10.1186/s12864-018-4970-9 |
| _version_ | 1818308593960615936 |
|---|---|
| author | C. Llorens S. C. Arcos L. Robertson R. Ramos R. Futami B. Soriano S. Ciordia M. Careche M. González-Muñoz Y. Jiménez-Ruiz N. Carballeda-Sangiao I. Moneo J. P. Albar M. Blaxter A. Navas |
| author_facet | C. Llorens S. C. Arcos L. Robertson R. Ramos R. Futami B. Soriano S. Ciordia M. Careche M. González-Muñoz Y. Jiménez-Ruiz N. Carballeda-Sangiao I. Moneo J. P. Albar M. Blaxter A. Navas |
| author_sort | C. Llorens |
| collection | DOAJ |
| description | Abstract Background Anisakis simplex sensu stricto and Anisakis pegreffii are sibling species of nematodes parasitic on marine mammals. Zoonotic human infection with third stage infective larvae causes anisakiasis, a debilitating and potentially fatal disease. These 2 species show evidence of hybridisation in geographical areas where they are sympatric. How the species and their hybrids differ is still poorly understood. Results Third stage larvae of Anisakis simplex s.s., Anisakis pegreffii and hybrids were sampled from Merluccius merluccius (Teleosti) hosts captured in waters of the FAO 27 geographical area. Specimens of each species and hybrids were distinguished with a diagnostic genetic marker (ITS). RNA was extracted from pools of 10 individuals of each taxon. Transcriptomes were generated using Illumina RNA-Seq, and assembled de novo. A joint assembly (here called merged transcriptome) of all 3 samples was also generated. The inferred transcript sets were functionally annotated and compared globally and also on subsets of secreted proteins and putative allergen families. While intermediary metabolism appeared to be typical for nematodes in the 3 evaluated taxa, their transcriptomes present strong levels of differential expression and enrichment, mainly of transcripts related to metabolic pathways and gene ontologies associated to energy metabolism and other pathways, with significant presence of excreted/secreted proteins, most of them allergens. The allergome of the 2 species and their hybrids has also been thoroughly studied; at least 74 different allergen families were identified in the transcriptomes. Conclusions A. simplex s.s., A. pegreffi and their hybrids differ in gene expression patterns in the L3 stage. Strong parent-of-origin effects were observed: A. pegreffi alleles dominate in the expression patterns of hybrids albeit the latter, and A. pegreffii also display significant differences indicating that hybrids are intermediate biological entities among their parental species, and thus of outstanding interest in the study of speciation in nematodes. Analyses of differential expression based on genes coding for secreted proteins suggests that co-infections presents different repertoires of released protein to the host environment. Both species and their hybrids, share more allergen genes than previously thought and are likely to induce overlapping disease responses. |
| first_indexed | 2024-12-13T07:16:45Z |
| format | Article |
| id | doaj.art-8027a2b243f64adfb4d05db6edbb24b2 |
| institution | Directory Open Access Journal |
| issn | 1471-2164 |
| language | English |
| last_indexed | 2024-12-13T07:16:45Z |
| publishDate | 2018-08-01 |
| publisher | BMC |
| record_format | Article |
| series | BMC Genomics |
| spelling | doaj.art-8027a2b243f64adfb4d05db6edbb24b22022-12-21T23:55:32ZengBMCBMC Genomics1471-21642018-08-0119112110.1186/s12864-018-4970-9Functional insights into the infective larval stage of Anisakis simplex s.s., Anisakis pegreffii and their hybrids based on gene expression patternsC. Llorens0S. C. Arcos1L. Robertson2R. Ramos3R. Futami4B. Soriano5S. Ciordia6M. Careche7M. González-Muñoz8Y. Jiménez-Ruiz9N. Carballeda-Sangiao10I. Moneo11J. P. Albar12M. Blaxter13A. Navas14Biotechvana, Scientific Park, University of ValenciaDepartamento Biodiversidad y Biología Evolutiva, Museo Nacional de Ciencias Naturales, CSICDepartamento Biodiversidad y Biología Evolutiva, Museo Nacional de Ciencias Naturales, CSICUnidad de Genómica, Campus de Cantoblanco, Scientific Park of MadridBiotechvana, Scientific Park, University of ValenciaBiotechvana, Scientific Park, University of ValenciaUnidad de Proteomica Centro Nacional de Biotecnología, CSICInstituto de Ciencia y Tecnología de Alimentos y Nutrición (ICTAN)Servicio de Immunología, Hospital Universitario La PazDepartamento Biodiversidad y Biología Evolutiva, Museo Nacional de Ciencias Naturales, CSICServicio de Immunología, Hospital Universitario La PazServicio de Immunología, Hospital Universitario La PazUnidad de Proteomica Centro Nacional de Biotecnología, CSICEdinburgh Genomics, and Institute of Evolutionary Biology, School of Biological Sciences, The King’s Buildings, The University of EdinburghDepartamento Biodiversidad y Biología Evolutiva, Museo Nacional de Ciencias Naturales, CSICAbstract Background Anisakis simplex sensu stricto and Anisakis pegreffii are sibling species of nematodes parasitic on marine mammals. Zoonotic human infection with third stage infective larvae causes anisakiasis, a debilitating and potentially fatal disease. These 2 species show evidence of hybridisation in geographical areas where they are sympatric. How the species and their hybrids differ is still poorly understood. Results Third stage larvae of Anisakis simplex s.s., Anisakis pegreffii and hybrids were sampled from Merluccius merluccius (Teleosti) hosts captured in waters of the FAO 27 geographical area. Specimens of each species and hybrids were distinguished with a diagnostic genetic marker (ITS). RNA was extracted from pools of 10 individuals of each taxon. Transcriptomes were generated using Illumina RNA-Seq, and assembled de novo. A joint assembly (here called merged transcriptome) of all 3 samples was also generated. The inferred transcript sets were functionally annotated and compared globally and also on subsets of secreted proteins and putative allergen families. While intermediary metabolism appeared to be typical for nematodes in the 3 evaluated taxa, their transcriptomes present strong levels of differential expression and enrichment, mainly of transcripts related to metabolic pathways and gene ontologies associated to energy metabolism and other pathways, with significant presence of excreted/secreted proteins, most of them allergens. The allergome of the 2 species and their hybrids has also been thoroughly studied; at least 74 different allergen families were identified in the transcriptomes. Conclusions A. simplex s.s., A. pegreffi and their hybrids differ in gene expression patterns in the L3 stage. Strong parent-of-origin effects were observed: A. pegreffi alleles dominate in the expression patterns of hybrids albeit the latter, and A. pegreffii also display significant differences indicating that hybrids are intermediate biological entities among their parental species, and thus of outstanding interest in the study of speciation in nematodes. Analyses of differential expression based on genes coding for secreted proteins suggests that co-infections presents different repertoires of released protein to the host environment. Both species and their hybrids, share more allergen genes than previously thought and are likely to induce overlapping disease responses.http://link.springer.com/article/10.1186/s12864-018-4970-9Anisakis simplexA. PegreffiiTranscriptomeAllergensGene expression |
| spellingShingle | C. Llorens S. C. Arcos L. Robertson R. Ramos R. Futami B. Soriano S. Ciordia M. Careche M. González-Muñoz Y. Jiménez-Ruiz N. Carballeda-Sangiao I. Moneo J. P. Albar M. Blaxter A. Navas Functional insights into the infective larval stage of Anisakis simplex s.s., Anisakis pegreffii and their hybrids based on gene expression patterns BMC Genomics Anisakis simplex A. Pegreffii Transcriptome Allergens Gene expression |
| title | Functional insights into the infective larval stage of Anisakis simplex s.s., Anisakis pegreffii and their hybrids based on gene expression patterns |
| title_full | Functional insights into the infective larval stage of Anisakis simplex s.s., Anisakis pegreffii and their hybrids based on gene expression patterns |
| title_fullStr | Functional insights into the infective larval stage of Anisakis simplex s.s., Anisakis pegreffii and their hybrids based on gene expression patterns |
| title_full_unstemmed | Functional insights into the infective larval stage of Anisakis simplex s.s., Anisakis pegreffii and their hybrids based on gene expression patterns |
| title_short | Functional insights into the infective larval stage of Anisakis simplex s.s., Anisakis pegreffii and their hybrids based on gene expression patterns |
| title_sort | functional insights into the infective larval stage of anisakis simplex s s anisakis pegreffii and their hybrids based on gene expression patterns |
| topic | Anisakis simplex A. Pegreffii Transcriptome Allergens Gene expression |
| url | http://link.springer.com/article/10.1186/s12864-018-4970-9 |
| work_keys_str_mv | AT cllorens functionalinsightsintotheinfectivelarvalstageofanisakissimplexssanisakispegreffiiandtheirhybridsbasedongeneexpressionpatterns AT scarcos functionalinsightsintotheinfectivelarvalstageofanisakissimplexssanisakispegreffiiandtheirhybridsbasedongeneexpressionpatterns AT lrobertson functionalinsightsintotheinfectivelarvalstageofanisakissimplexssanisakispegreffiiandtheirhybridsbasedongeneexpressionpatterns AT rramos functionalinsightsintotheinfectivelarvalstageofanisakissimplexssanisakispegreffiiandtheirhybridsbasedongeneexpressionpatterns AT rfutami functionalinsightsintotheinfectivelarvalstageofanisakissimplexssanisakispegreffiiandtheirhybridsbasedongeneexpressionpatterns AT bsoriano functionalinsightsintotheinfectivelarvalstageofanisakissimplexssanisakispegreffiiandtheirhybridsbasedongeneexpressionpatterns AT sciordia functionalinsightsintotheinfectivelarvalstageofanisakissimplexssanisakispegreffiiandtheirhybridsbasedongeneexpressionpatterns AT mcareche functionalinsightsintotheinfectivelarvalstageofanisakissimplexssanisakispegreffiiandtheirhybridsbasedongeneexpressionpatterns AT mgonzalezmunoz functionalinsightsintotheinfectivelarvalstageofanisakissimplexssanisakispegreffiiandtheirhybridsbasedongeneexpressionpatterns AT yjimenezruiz functionalinsightsintotheinfectivelarvalstageofanisakissimplexssanisakispegreffiiandtheirhybridsbasedongeneexpressionpatterns AT ncarballedasangiao functionalinsightsintotheinfectivelarvalstageofanisakissimplexssanisakispegreffiiandtheirhybridsbasedongeneexpressionpatterns AT imoneo functionalinsightsintotheinfectivelarvalstageofanisakissimplexssanisakispegreffiiandtheirhybridsbasedongeneexpressionpatterns AT jpalbar functionalinsightsintotheinfectivelarvalstageofanisakissimplexssanisakispegreffiiandtheirhybridsbasedongeneexpressionpatterns AT mblaxter functionalinsightsintotheinfectivelarvalstageofanisakissimplexssanisakispegreffiiandtheirhybridsbasedongeneexpressionpatterns AT anavas functionalinsightsintotheinfectivelarvalstageofanisakissimplexssanisakispegreffiiandtheirhybridsbasedongeneexpressionpatterns |