The Mitochondrial Genomes of the Zoonotic Canine Filarial Parasites Dirofilaria (Nochtiella) repens and Candidatus Dirofilaria (Nochtiella) Honkongensis Provide Evidence for Presence of Cryptic Species

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Abstract

Background

Cutaneous dirofilariosis is a canine mosquito-borne zoonosis that can cause larva migrans disease in humans. Dirofilaria repens is considered an emerging pathogen occurring with high prevalence in Mediterranean areas and many parts of tropical Asia. In Hong Kong, a second species, Candidatus Dirofilaria hongkongensis, has been reported. The present study aimed to compare mitochondrial genomes from these parasites and to obtain population genetic information.

Methods and Findings

Complete mitochondrial genomes were obtained by PCR and Sanger sequencing or ILLUMINA sequencing for four worms. Cytochrome oxidase subunit 1 sequences identified three as D. repens (all from Europe) and one as C. D. hongkongensis (from India). Mitochondrial genomes have the same organization as in other spirurid nematodes but a higher preference for thymine in the coding strand. Phylogenetic analysis was in contradiction to current taxonomy of the Onchocercidae but in agreement with a recent multi-locus phylogenetic analysis using both mitochondrial and nuclear markers. D. repens and C. D. hongkongensis sequences clustered together and were the common sister group to Dirofilaria immitis. Analysis of a 2.5 kb mitochondrial genome fragment from macrofilaria or canine blood samples from Europe (42), Thailand (2), India (1) and Vietnam (1) revealed only small genetic differences in the D. repens samples including all European and the Vietnam sample. The Indian C. D. hongkongensis and the two Thai samples formed separate clusters and differences were comparatively large.

Conclusion

Genetic differences between Dirofilaria spp. causing cutaneous disease can be considerable whereas D. repens itself was genetically quite homogenous. C. D. hongkongensis was identified for the first time from the Indian subcontinent. The full mitochondrial genome sequence strengthens the hypothesis that it represents an independent species and the Thai samples might represent another cryptic species, Candidatus Dirofilaria sp. ‘Thailand II’, or a quite divergent population of C. D. hongkongensis.

Author Summary

The mitochondrial genomes of the zoonotic parasite species Dirofilaria repens and Candidatus Dirofilaria hongkongensis were characterized and compared to the genomes of other filariae. The resulting phylogeny is largely in agreement with recent molecular data. C. D. hongkongensis was placed as a sister group to D. repens and both as a common sister to D. immitis. The large genetic difference between D. repens and C. D. hongkongensis further supports the hypothesis that both are distinct valid species. Two canine samples from Thailand that were diagnosed as D. repens are either from a C. D. hongkongensis population that is quite divergent from the Indian population or might represent another currently unrecognized species in the genus.

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Most cited references 61

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Human and animal dirofilariasis: the emergence of a zoonotic mosaic.

Fernando Simón, Mar Siles-Lucas, Rodrigo Morchón … (2012)

Dirofilariasis represents a zoonotic mosaic, which includes two main filarial species (Dirofilaria immitis and D. repens) that have adapted to canine, feline, and human hosts with distinct biological and clinical implications. At the same time, both D. immitis and D. repens are themselves hosts to symbiotic bacteria of the genus Wolbachia, the study of which has resulted in a profound shift in the understanding of filarial biology, the mechanisms of the pathologies that they produce in their hosts, and issues related to dirofilariasis treatment. Moreover, because dirofilariasis is a vector-borne transmitted disease, their distribution and infection rates have undergone significant modifications influenced by global climate change. Despite advances in our knowledge of D. immitis and D. repens and the pathologies that they inflict on different hosts, there are still many unknown aspects of dirofilariasis. This review is focused on human and animal dirofilariasis, including the basic morphology, biology, protein composition, and metabolism of Dirofilaria species; the climate and human behavioral factors that influence distribution dynamics; the disease pathology; the host-parasite relationship; the mechanisms involved in parasite survival; the immune response and pathogenesis; and the clinical management of human and animal infections.

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An index of substitution saturation and its application.

Xuhua Xia, Zheng Xie, Marco Salemi … (2003)

We introduce a new index to measure substitution saturation in a set of aligned nucleotide sequences. The index is based on the notion of entropy in information theory. We derive the critical values of the index based on computer simulation with different sequence lengths, different number of OTUs and different topologies. The critical value enables researchers to quickly judge whether a set of aligned sequences is useful in phylogenetics. We illustrate the index by applying it to an analysis of the aligned sequences of the elongation factor-1alpha gene originally used to resolve the deep phylogeny of major arthropod groups. The method has been implemented in DAMBE.

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Is Open Access

FASconCAT-G: extensive functions for multiple sequence alignment preparations concerning phylogenetic studies

Patrick Kück, Gary C Longo (2014)

Background Phylogenetic and population genetic studies often deal with multiple sequence alignments that require manipulation or processing steps such as sequence concatenation, sequence renaming, sequence translation or consensus sequence generation. In recent years phylogenetic data sets have expanded from single genes to genome wide markers comprising hundreds to thousands of loci. Processing of these large phylogenomic data sets is impracticable without using automated process pipelines. Currently no stand-alone or pipeline compatible program exists that offers a broad range of manipulation and processing steps for multiple sequence alignments in a single process run. Results Here we present FASconCAT-G, a system independent editor, which offers various processing options for multiple sequence alignments. The software provides a wide range of possibilities to edit and concatenate multiple nucleotide, amino acid, and structure sequence alignment files for phylogenetic and population genetic purposes. The main options include sequence renaming, file format conversion, sequence translation between nucleotide and amino acid states, consensus generation of specific sequence blocks, sequence concatenation, model selection of amino acid replacement with ProtTest, two types of RY coding as well as site exclusions and extraction of parsimony informative sites. Convieniently, most options can be invoked in combination and performed during a single process run. Additionally, FASconCAT-G prints useful information regarding alignment characteristics and editing processes such as base compositions of single in- and outfiles, sequence areas in a concatenated supermatrix, as well as paired stem and loop regions in secondary structure sequence strings. Conclusions FASconCAT-G is a command-line driven Perl program that delivers computationally fast and user-friendly processing of multiple sequence alignments for phylogenetic and population genetic applications and is well suited for incorporation into analysis pipelines. Electronic supplementary material The online version of this article (doi:10.1186/s12983-014-0081-x) contains supplementary material, which is available to authorized users.

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Author and article information

Contributors

Benjamin L Makepeace: Role: Editor

Journal

Journal ID (nlm-ta): PLoS Negl Trop Dis

Journal ID (iso-abbrev): PLoS Negl Trop Dis

Journal ID (publisher-id): plos

Journal ID (pmc): plosntds

Title: PLoS Neglected Tropical Diseases

Publisher: Public Library of Science (San Francisco, CA USA )

ISSN (Print): 1935-2727

ISSN (Electronic): 1935-2735

Publication date (Electronic): 11 October 2016

Publication date Collection: October 2016

Volume: 10

Issue: 10

Electronic Location Identifier: e0005028

Affiliations

[1 ]Institute for Parasitology and Tropical Veterinary Medicine, Freie Universität Berlin, Berlin, Germany

[2 ]Institute of Medical Microbiology, Justus-Liebig-University, Giessen, Germany; German Center for Infection Research (DZIF), Partner site Giessen-Marburg-Langen, Campus Giessen, Giessen, Germany

[3 ]IDEXX Laboratories, Ludwigsburg, Germany

[4 ]Institut für Parasitologie, Universität Leipzig, Leipzig, Germany

[5 ]Department of Parasitology, Faculty of Medicine Siriraj Hospital, Mahidol University, Bangkok, Thailand

[6 ]Department of Veterinary Medicine, University of Bari, Bari, Italy

[7 ]Division of Infectious Diseases and Tropical Medicine, Medical Centre of the University of Munich (LMU); German Center for Infection Research (DZIF), Partner site Munich, Germany

[8 ]Section Clinical Tropical Medicine, Department of Infectious Diseases, Heidelberg University Hospital, Heidelberg, Germany

[9 ]Immunology Department, Institute of Biotechnology, Ha Noi, Viet Nam

[10 ]Department of Parasitology, Viet Nam Veterinary Medical University, Ha Noi, Viet Nam

[11 ]Bayer Animal Health GmbH, Monheim, Germany

[12 ]University Medical Center, Hamburg-Eppendorf, Germany

University of Liverpool, UNITED KINGDOM

Author notes

I have read the journal's policy and the authors of this manuscript have the following competing interests: RS is an employee of Bayer Animal Health, a company that produces and sells anti-parasitic drugs. NP is an employee of IDEXX Laboraroties, a company that provides veterinary diagnostic Services including diagnosis of Dirofilaria spp. With the exception of RS and NP, Bayer Animal Health and IDEXX Laboratories were not involved in study design, data collection, data analysis or preparation of the manuscript. The decision to publish the manuscript was jointly taken. This does not alter our adherence to all PLOS policies on sharing data and materials.

Conceptualization: JK SP GvSH RS MF EY.
Data curation: EY JK MF.
Formal analysis: JK MF EY.
Funding acquisition: GvSH SP RS.
Investigation: EY MF ML NP SW SR DO.
Methodology: EY MF JK.
Project administration: GvSH SP JK.
Resources: NP DO SW IK MD THL TAL RS.
Software: MF.
Supervision: JK SP GvSH.
Validation: EY MF SP SR JK.
Visualization: JK EY.
Writing – original draft: JK EY SP MF GvSH NP DO.
Writing – review & editing: JK EY MF SP.

* E-mail: juergen.kruecken@ 123456fu-berlin.de

Article

Publisher ID: PNTD-D-16-00976

DOI: 10.1371/journal.pntd.0005028

PMC ID: 5058507

PubMed ID: 27727270

SO-VID: 5dc475eb-bed6-4abd-b6ca-dc00adb79c77

License:

This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

History

Date received : 3 June 2016

Date accepted : 9 September 2016

Page count

Figures: 4, Tables: 1, Pages: 22

Funding

Funded by: Bayer Animal Health

Award Recipient : Esra Yilmaz

The present study was partially performed as a collaborative research project between Bayer Animal Health and the Institute of Parasitology and Tropical Veterinary Medicine, Freie Universität Berlin. Other parts were conducted without external support at the Justus-Liebig-University, Gießen. The funders had no role in study design, data collection and analysis, or preparation of the manuscript. The decision to publish the manuscript was jointly taken.

Custom metadata

Data Availability All sequence data are available from the GenBank database (accession number(s) KX265047-KX265093).

The Mitochondrial Genomes of the Zoonotic Canine Filarial Parasites Dirofilaria ( Nochtiella) repens and Candidatus Dirofilaria (Nochtiella) Honkongensis Provide Evidence for Presence of Cryptic Species

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Abstract

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Most cited references 61

Human and animal dirofilariasis: the emergence of a zoonotic mosaic.

An index of substitution saturation and its application.

FASconCAT-G: extensive functions for multiple sequence alignment preparations concerning phylogenetic studies

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