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      Description, molecular characteristics and Wolbachia endosymbionts of Onchocerca borneensis Uni, Mat Udin & Takaoka n. sp. (Nematoda: Filarioidea) from the Bornean bearded pig Sus barbatus Müller (Cetartiodactyla: Suidae) of Sarawak, Malaysia

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          Abstract

          Background

          The genus Onchocerca Diesing, 1841 includes species of medical importance, such as O. volvulus (Leuckart, 1893), which causes river blindness in the tropics. Recently, zoonotic onchocercosis has been reported in humans worldwide. In Japan, O. dewittei japonica Uni, Bain & Takaoka, 2001 from wild boars is a causative agent for this zoonosis. Many filarioid nematodes are infected with Wolbachia endosymbionts which exhibit various evolutionary relationships with their hosts. While investigating the filarial fauna of Borneo, we discovered an undescribed Onchocerca species in the bearded pig Sus barbatus Müller (Cetartiodactyla: Suidae).

          Methods

          We isolated Onchocerca specimens from bearded pigs and examined their morphology. For comparative material, we collected fresh specimens of O. d. dewittei Bain, Ramachandran, Petter & Mak, 1977 from banded pigs ( S. scrofa vittatus Boie) in Peninsular Malaysia. Partial sequences of three different genes (two mitochondrial genes, cox1 and 12S rRNA, and one nuclear ITS region) of these filarioids were analysed. By multi-locus sequence analyses based on six genes ( 16S rDNA, ftsZ, dnaA, coxA, fbpA and gatB) of Wolbachia, we determined the supergroups in the specimens from bearded pigs and those of O. d. dewittei.

          Results

          Onchocerca borneensis Uni, Mat Udin & Takaoka n. sp. is described on the basis of morphological characteristics and its genetic divergence from congeners. Molecular characteristics of the new species revealed its close evolutionary relationship with O. d. dewittei. Calculated p-distance for the cox1 gene sequences between O. borneensis n. sp. and O. d. dewittei was 5.9%, while that between O. d. dewittei and O. d. japonica was 7.6%. No intraspecific genetic variation was found for the new species. Wolbachia strains identified in the new species and O. d. dewittei belonged to supergroup C and are closely related.

          Conclusions

          Our molecular analyses of filarioids from Asian suids indicate that the new species is sister to O. d. dewittei. On the basis of its morphological and molecular characteristics, we propose to elevate O. d. japonica to species level as O. japonica Uni, Bain & Takaoka, 2001. Coevolutionary relationships exist between the Wolbachia strains and their filarial hosts in Borneo and Peninsular Malaysia.

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          Most cited references49

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          Wolbachia as a bacteriocyte-associated nutritional mutualist.

          Many insects are dependent on bacterial symbionts that provide essential nutrients (ex. aphid-Buchnera and tsetse-Wiglesworthia associations), wherein the symbionts are harbored in specific cells called bacteriocytes that constitute a symbiotic organ bacteriome. Facultative and parasitic bacterial symbionts like Wolbachia have been regarded as evolutionarily distinct from such obligate nutritional mutualists. However, we discovered that, in the bedbug Cimex lectularius, Wolbachia resides in a bacteriome and appears to be an obligate nutritional mutualist. Two bacterial symbionts, a Wolbachia strain and an unnamed gamma-proteobacterium, were identified from different strains of the bedbug. The Wolbachia symbiont was detected from all of the insects examined whereas the gamma-proteobacterium was found in a part of them. The Wolbachia symbiont was specifically localized in the bacteriomes and vertically transmitted via the somatic stem cell niche of germalia to oocytes, infecting the incipient symbiotic organ at an early stage of the embryogenesis. Elimination of the Wolbachia symbiont resulted in retarded growth and sterility of the host insect. These deficiencies were rescued by oral supplementation of B vitamins, confirming the essential nutritional role of the symbiont for the host. The estimated genome size of the Wolbachia symbiont was around 1.3 Mb, which was almost equivalent to the genome sizes of parasitic Wolbachia strains of other insects. These results indicate that bacteriocyte-associated nutritional mutualism can evolve from facultative and prevalent microbial associates like Wolbachia, highlighting a previously unknown aspect of the parasitism-mutualism evolutionary continuum.
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            Wolbachia bacterial endosymbionts of filarial nematodes.

            Filarial nematodes are important helminth parasites of the tropics and a leading cause of global disability. They include species responsible for onchocerciasis, lymphatic filariasis and dirofilariasis. A unique feature of these nematodes is their dependency upon a symbiotic intracellular bacterium, Wolbachia, which is essential for normal development and fertility. Advances in our understanding of the symbiosis of Wolbachia bacteria with filarial nematodes have made rapid progress in recent years. Here we summarise our current understanding of the evolution of the symbiotic association together with insights into the functional basis of the interaction derived from genomic analysis. Also we discuss the contribution of Wolbachia to inflammatory-mediated pathogenesis and adverse reactions to anti-filarial drugs and describe the outcome of recent field trials using antibiotics as a promising new tool for the treatment of filarial infection and disease.
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              Vector-borne helminths of dogs and humans in Europe

              Presently, 45% of the total human population of Europe, as well as their domestic and companion animals, are exposed to the risk of vector-borne helminths (VBH) causing diseases. A plethora of intrinsic biological and extrinsic factors affect the relationship among helminths, vectors and animal hosts, in a constantly changing environment. Although canine dirofilarioses by Dirofilaria immitis and Dirofilaria repens are key examples of the success of VBH spreading into non-endemic areas, another example is represented by Thelazia callipaeda eyeworm, an emergent pathogen of dogs, cats and humans in several regions of Europe. The recent finding of Onchocerca lupi causing canine and human infestation in Europe and overseas renders the picture of VBH even more complicated. Similarly, tick-transmitted filarioids of the genus Cercopithifilaria infesting the skin of dogs were recently shown to be widespread in Europe. Although for most of the VBH above there is an increasing accumulation of research data on their distribution at national level, the overall impact of the diseases they cause in dogs and humans is not fully recognised in many aspects. This review investigates the reasons underlying the increasing trend in distribution of VBH in Europe and discusses the diagnostic and control strategies currently available. In addition, this article provides the authors’ opinion on some topics related to VBH that would deserve further scientific investigation.
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                Author and article information

                Contributors
                unishigehiko@um.edu.my , uni@med.osaka-cu.ac.jp
                akifsirhan@gmail.com
                agatsuma@kochi-u.ac.jp
                JunkerK@arc.agric.za
                weerachai.s@msu.ac.th
                aoy_narumon@hotmail.com
                mfukuda@oita-u.ac.jp
                coralie.martin@mnhn.fr
                elefoulon@neb.com
                alabat@mnhn.fr
                fanwaral@gmail.com
                vanlun_low@um.edu.my
                cheahpl@um.edu.my
                limailian@um.edu.my
                rosliramli@um.edu.my
                daicus@yahoo.com
                afiquahzainuri@gmail.com
                matsubayashi@vet.osakafu-u.ac.jp
                zaiti_1978@um.edu.my
                subhabhassu@um.edu.my
                s-uga@yg.kobe-wu.ac.jp
                roslihashim@um.edu.my
                takaoka@oita-u.ac.jp
                sofian@um.edu.my
                Journal
                Parasit Vectors
                Parasit Vectors
                Parasites & Vectors
                BioMed Central (London )
                1756-3305
                6 February 2020
                6 February 2020
                2020
                : 13
                : 50
                Affiliations
                [1 ]ISNI 0000 0001 2308 5949, GRID grid.10347.31, Institute of Biological Sciences, Faculty of Science, , University of Malaya, ; 50603 Kuala Lumpur, Malaysia
                [2 ]ISNI 0000 0001 0707 9143, GRID grid.411103.6, Department of Public Health, Faculty of Nursing, , Kobe Women’s University, ; Kobe, 650-0046 Japan
                [3 ]ISNI 0000 0001 0659 9825, GRID grid.278276.e, Department of Environmental Medicine, Kochi Medical School, , Kochi University, ; Nankoku, 783-8505 Japan
                [4 ]ISNI 0000 0001 0691 4346, GRID grid.452772.1, ARC-Onderstepoort Veterinary Institute, ; Private Bag X05, Onderstepoort, 0110 South Africa
                [5 ]ISNI 0000 0001 1887 7220, GRID grid.411538.a, Walai Rukhavej Botanical Research Institute, Mahasarakham University, ; Maha Sarakham, 44150 Thailand
                [6 ]ISNI 0000 0001 0665 3553, GRID grid.412334.3, Institute for Research Promotion, , Oita University, ; Oita, 879-5593 Japan
                [7 ]ISNI 0000 0001 2174 9334, GRID grid.410350.3, UMR7245, MCAM, , Muséum National d’Histoire Naturelle, ; 75005 Paris, France
                [8 ]ISNI 0000 0004 0376 1796, GRID grid.273406.4, Molecular Parasitology Group, , New England Biolabs, Inc, ; Ipswich, MA 01938 USA
                [9 ]ISNI 0000 0000 9534 9846, GRID grid.412253.3, Department of Zoology, Faculty of Resource Sciences and Technology, , Universiti Malaysia Sarawak, ; 943800 Kota Samarahan, Sarawak Malaysia
                [10 ]ISNI 0000 0001 2308 5949, GRID grid.10347.31, Tropical Infectious Diseases Research & Education Centre, , University of Malaya, ; 50603 Kuala Lumpur, Malaysia
                [11 ]ISNI 0000 0001 2308 5949, GRID grid.10347.31, Department of Pathology, Faculty of Medicine, , University of Malaya, ; 50603 Kuala Lumpur, Malaysia
                [12 ]ISNI 0000 0001 2308 5949, GRID grid.10347.31, Department of Parasitology, Faculty of Medicine, , University of Malaya, ; 50603 Kuala Lumpur, Malaysia
                [13 ]ISNI 0000 0001 0676 0594, GRID grid.261455.1, Department of International Prevention of Epidemics, Division of Veterinary Science, Graduate School of Life and Environmental Sciences, , Osaka Prefecture University, ; Osaka, 598-8531 Japan
                [14 ]ISNI 0000 0001 2308 5949, GRID grid.10347.31, Centre for Biotechnology in Agriculture, CEBAR, , University of Malaya, ; 50300 Kuala Lumpur, Malaysia
                Article
                3907
                10.1186/s13071-020-3907-8
                7006428
                32028994
                11c80395-1487-4830-8925-097ecbec6cd2
                © The Author(s) 2020

                Open AccessThis 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/. The Creative Commons Public Domain Dedication waiver ( http://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.

                History
                : 29 August 2019
                : 15 January 2020
                Funding
                Funded by: The Ministry of Higher Education, Malaysia
                Award ID: FRGS EP020-2012
                Award Recipient :
                Categories
                Research
                Custom metadata
                © The Author(s) 2020

                Parasitology
                coevolution,indomalayan realm,malayfilaria sofiani,onchocerca dewittei,onchocerca japonica,suidae

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