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.
Coevolution
Indomalayan realm
Malayfilaria sofiani
Onchocerca dewittei
Onchocerca japonica
Suidae
Journal
Parasites & vectors
ISSN: 1756-3305
Titre abrégé: Parasit Vectors
Pays: England
ID NLM: 101462774
Informations de publication
Date de publication:
06 Feb 2020
06 Feb 2020
Historique:
received:
29
08
2019
accepted:
15
01
2020
entrez:
8
2
2020
pubmed:
8
2
2020
medline:
6
6
2020
Statut:
epublish
Résumé
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). 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. 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. 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.
Sections du résumé
BACKGROUND
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
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
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
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.
Identifiants
pubmed: 32028994
doi: 10.1186/s13071-020-3907-8
pii: 10.1186/s13071-020-3907-8
pmc: PMC7006428
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
50Subventions
Organisme : The Ministry of Higher Education, Malaysia
ID : FRGS EP020-2012
Références
Parasite. 2002 Dec;9(4):293-304
pubmed: 12514943
Parasite. 2004 Sep;11(3):285-92
pubmed: 15490753
Parasit Vectors. 2017 Apr 20;10(1):194
pubmed: 28427478
Mol Ecol. 1999 Sep;8(9):1509-12
pubmed: 10564456
Parasitology. 2001 Jan;122 Pt 1:93-103
pubmed: 11197770
Parasit Vectors. 2013 Jan 16;6:16
pubmed: 23324440
Mol Biol Evol. 2002 Mar;19(3):341-6
pubmed: 11861893
Genome Biol. 2013;14(9):R107
pubmed: 24070215
Adv Parasitol. 2005;60:245-84
pubmed: 16230105
Zookeys. 2012;(219):1-10
pubmed: 22977348
Parasite. 2008 Sep;15(3):342-8
pubmed: 18814705
Emerg Infect Dis. 2007 Nov;13(11):1749-52
pubmed: 18217562
J Helminthol. 2014 Jun;88(2):250-5
pubmed: 23388686
PLoS One. 2012;7(6):e38544
pubmed: 22685581
Acta Trop. 2007 Jan;101(1):1-14
pubmed: 17174932
Parasitol Int. 2005 Sep;54(3):195-9
pubmed: 15936981
Int J Parasitol. 1994 Dec;24(8):1179-201
pubmed: 7729976
Parasite. 2018;25:50
pubmed: 30234481
Parasitol Res. 2003 Mar;89(5):381-6
pubmed: 12632152
Infect Genet Evol. 2009 Sep;9(5):748-59
pubmed: 19539785
Am J Trop Med Hyg. 2013 Mar;88(3):601-5
pubmed: 23382171
Am J Trop Med Hyg. 2011 Jan;84(1):55-8
pubmed: 21212202
Microbes Infect. 2003 Apr;5(4):261-73
pubmed: 12706439
Proc Natl Acad Sci U S A. 2010 Jan 12;107(2):769-74
pubmed: 20080750
Biol Open. 2012 Jun 15;1(6):536-47
pubmed: 23213446
Front Zool. 2009 Jan 07;6:1
pubmed: 19128479
PeerJ. 2016 Mar 28;4:e1840
pubmed: 27069790
Science. 2005 Mar 11;307(5715):1618-21
pubmed: 15761152
Int J Parasitol. 2017 Jul;47(8):457-470
pubmed: 28344097
Parasit Vectors. 2015 Jan 27;8:59
pubmed: 25623081
Ann Parasitol Hum Comp. 1981;56(5):503-26
pubmed: 7332196
Mol Biol Evol. 2015 Jan;32(1):268-74
pubmed: 25371430
Parasitol Int. 2019 Oct;72:101943
pubmed: 31220633
Parasite. 2007 Sep;14(3):199-211
pubmed: 17933297
Annu Rev Anim Biosci. 2016;4:61-85
pubmed: 26526544
Parasitol Int. 2015 Dec;64(6):493-502
pubmed: 26165205
Parasite. 2006 Sep;13(3):193-200
pubmed: 17007210
PLoS One. 2011;6(6):e20843
pubmed: 21731626
Vet Parasitol. 2011 Nov 24;182(1):14-21
pubmed: 21852040
Ophthalmology. 1998 Aug;105(8):1494-7
pubmed: 9709764
Nat Methods. 2017 Jun;14(6):587-589
pubmed: 28481363
Mol Biol Evol. 2016 Jul;33(7):1870-4
pubmed: 27004904
Mol Biochem Parasitol. 2018 Jul;223:31-36
pubmed: 29964059
Brief Bioinform. 2008 Jul;9(4):286-98
pubmed: 18372315
Int J Parasitol. 2012 Oct;42(11):1025-36
pubmed: 23041355
Am J Trop Med Hyg. 1974 Jul;23(4):595-607
pubmed: 4847039
Ann Parasitol Hum Comp. 1977 Jul-Aug;52(4):471-9
pubmed: 931324
PLoS Negl Trop Dis. 2015 Nov 20;9(11):e0004233
pubmed: 26588229
Parasite. 2001 Sep;8(3):215-22
pubmed: 11584751
Parasitol Int. 2010 Sep;59(3):477-80
pubmed: 20561913