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Molecular Characterisation of Bulinus Snails – Intermediate Hosts of Schistosomes in Ogun State, South-Western Nigeria

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Molecular Characterisation of Bulinus Snails – Intermediate Hosts of Schistosomes in Ogun State, South-Western Nigeria Folia Malacol. 23: 137–147 http://dx.doi.org/10.12657/folmal.023.009 MOLECULAR CHARACTERISATION OF BULINUS SNAILS – INTERMEDIATE HOSTS OF SCHISTOSOMES IN OGUN STATE, SOUTH-WESTERN NIGERIA OLAOLUWA AKINWALE1,*, OPEYEMI OSO2, OYETUNDE SALAWU3, ALEXANDER ODAIBO2, PETRUS TANG4, TING-WEN CHEN5, PAM GYANG1 1 Molecular Parasitology Research Laboratory, Public Health Division, Nigerian Institute of Medical Research, Yaba, Lagos, Nigeria (e-mail: [email protected], [email protected]) 2 Parasitology Research Unit, Department of Zoology, University of Ibadan, Ibadan, Nigeria (e-mail: [email protected], [email protected]) 3 Department of Biosciences and Biotechnology, Babcock University, Ilishan, Ilishan-Remo, Nigeria (e-mail: [email protected]) 4 Molecular Regulation and Bioinformatics Laboratory, Department of Parasitology, College of Medicine, Chang Gung University, Kweishan, Taoyuan, Taiwan (e-mail: [email protected]) 5 Bioinformatics Core Laboratory, Molecular Medicine Research Centre, Chang Gung University, Kweishan, Taoyuan, Taiwan (e-mail: [email protected]) *corresponding author ABSTRACT: Freshwater snails of the genus Bulinus O. F. Müller, 1781 are intermediate hosts for schistosomes, trematode parasites which cause schistosomiasis. The genus includes closely related species complexes with restricted gene flow between populations of each taxon. Despite their importance as intermediate hosts, unambiguous identification of these snails remains challenging. We applied molecular approach to their identification to achieve a better understanding of the epidemiology of schistosomiasis in an endemic region, south-western Nigeria. A total of 149 snails were collected and their genomic DNA was screened for schistosome infection using PCR amplification of schistosome DraI repeat sequence. The snails were identified by PCR-RFLP and/or sequencing of an amplicon of their entire ITS region including the 5.8S ribosomal RNA (rRNA) gene. Four Bulinus species, namely B. globosus (Morelet, 1866), B. forskalii (Ehrenberg, 1831), B. camerunensis Mandahl-Barth, 1957 and B. senegalensis O. F. Müller, 1781 were identified, and 34.9% (n = 52) of the 149 snails were infected: B. globosus 25.5% (n = 38), B. forskalii 5.4% (n = 8), B. camerunensis 2.7% (n = 4) and B. senegalensis 1.3% (n = 2). Restriction fragment profiles of the ribosomal ITS region for B. globosus closely matched those obtained in our previous study thus confirming the view that ribosomal ITS region of these snails could be well suited for taxonomic studies. The use of sequencing for species identification was costly and time-consuming, but it was effective in resolving true identities of snails whose restriction profiles were similar and inconclusive. KEY WORDS: species identification, Bulinus, ITS, rRNA gene, schistosome, schistosomiasis, Nigeria INTRODUCTION Schistosomiasis, an infection caused by blood 1989, MAFE et al. 2000, OFOEZIE 2002, OGBE 2002), flukes of the genusSchistosoma Weinland, 1858, is en- and an estimated 33.5 million people, mainly chil- demic in Nigeria (AKOGUN & AKOGUN 1996, MAFE dren aged 5–19 years, are at risk (HOTEZ & KAMATH et al. 2000). Both Schistosoma haematobium (Bilharz, 2009). Freshwater pulmonates of the genera Bulinus 1852) and S. mansoni Sambon, 1907 infections oc- O. F. Müller, 1781 and Biomphalaria Preston, 1910 cur in all the states of the federation (EJEZIE et al. act as intermediate hosts for the parasites; the snails 138 Olaoluwa Akinwale et al. occur commonly throughout much of Africa and its AJAYI (2007) recorded five medically important snail adjacent regions. Their focal distribution has been species comprising B. globosus, B. truncatus, B. forskalii, reported in many parts of Nigeria (OKWUOSA & B. pfeifferi, and Radix natalensis (Krauss, 1848) in two UKOLI 1980, IMEVBORE et al. 1988, NDIFON & UKOLI Local Government Areas of Bauchi State, north-east- 1989, OFOEZIE 1999, OWOJORI et al. 2006) where ern Nigeria. It is noteworthy that in all these studies Biomphalaria pfeifferi (Krauss, 1848), Bulinus globosus the snail identification was based on morphological (Morelet, 1866) and B. truncatus (Audouin, 1827) characters. were recorded from diverse freshwater habitats. Correct identification of Bulinus species based on Urinary schistosomiasis is caused by S. haematobium, morphology alone may be difficult (RAAHAUGE et with some snails of the genus Bulinus acting as the al. 1984), since the morphological distinctiveness intermediate hosts. Among the intermediate hosts of within these species groups is limited. There are 37 S. haematobium, B. globosus was reported to be widely recognised species of the genus Bulinus divided into distributed and common while B. truncatus was rare. four major species groups, namely B. forskalii, B. afri­ IMEVBORE et al. (1988), NDIFON & UKOLI (1989), canus, B. truncatus/tropicus complex and B. reticulatus OFOEZIE (1999), NALE et al. (2003) and OWOJORI et (BROWN 1994). Within each of these groups, there al. (2006) reported the presence of B. globosus and B. are species that act as intermediate hosts for schisto- truncatus in the River Kibanni, at Zaria, north-west- somes in part or all of their geographical range, while ern Nigeria. BETTERTON et al. (1988) investigat- the specificity of the snail-parasite interaction is such ed 165 freshwater habitats throughout Kano state, that only certain species are involved in transmission north-western Nigeria, and recorded a number of of the parasite (ROLLINSON et al. 1998). Since the potential intermediate host species: Bulinus senegalen­ interaction between schistosomes and snails is very sis O. F. Müller, 1781, B. forskalii (Ehrenberg, 1831), specific, and compatibility may differ over fairly small B. globosus, B. truncatus and Biomphalaria pfeifferi; the geographical ranges, a reliable taxonomy of the genus most widespread was B. senegalensis. NTONIFOR & Bulinus is a prerequisite for understanding the epi- Fig. 1. Map of Yewa North LGA, Ogun state, Nigeria, showing the study areas Molecular characterisation of Bulinus species from Ogun, Nigeria 139 demiology of schistosome infection. Consequently, amplified polymorphic DNA (RAPDs), ITS2 second- considerable efforts have been focused on providing ary structure and sequence analysis of mitochondri- reliable methods for their differentiation and iden- al genes (SIMPSON et al. 1984, ROLLINSON & KANE tification in order to specify the species and strains 1991, JOHNSTON et al. 1993, KANE & ROLLINSON playing a major role in the disease transmission. The 1994, STOTHARD et al. 1996, 1997, 2001, STOTHARD studies of ploidy (GOLDMAN et al. 1983) and al- & ROLLINSON 1997, RAAHAUGE & KRISTENSEN 2000, lozymes (ROLLINSON & SOUTHGATE 1979, NASCETTI JONES et al. 2001, JØRGENSEN et al. 2007, 2011, 2013, & BULLINI 1980, MIMPFOUNDI & GREER 1989) have KANE et al. 2008, AKINWALE et al. 2011, NALUGWA et played an increasing role in Bulinus species iden- al. 2011, NYAKAANA et al. 2013) have recently been tification in addition to enzyme electrophoresis applied to Bulinus species identification. This study (BIOCCA et al. 1979, JELNES 1979, 1986, ROLLINSON therefore aimed to characterise Bulinus species in- & SOUTHGATE 1979, NJIOKOU et al. 1993). Various volved in schistosome transmission in an endemic molecular methods such as PCR amplification of the region, south-western Nigeria through PCR-RFLP snails’ ribosomal ITS region and restriction fragment and/or sequencing of amplicons of the snails’ entire length polymorphism (RFLP), the use of randomly ribosomal ITS region. AREAS STUDIED Five rivers running through nine rural commu- (Table 1) are fishing and farming. They suffer from nities in Yewa North Local Government Area (LGA) endemic urinary schistosomiasis. Yewa North LGA, of Ogun state, south-western Nigeria (Fig. 1), were located at 7°15’N and 3°03’E in a deciduous/derived surveyed for freshwater snails of the genus Bulinus. savannah zone, has the largest land area in the state The main occupations of the people in the area (ONAKOMAYA et al. 1992). Table 1. Geographical coordinates, sample origins, number of snails collected and prevalence of schistosome infection Location River GPS coordinates No. of snails screened No. infected Prevalence of infection (%) 1 Imasayi Iju 7°05’N, 3°05’E 34 7 20.6 2 Eggua Idi 7°00’N, 2°54’E 3 3 100.0 3 Ijale Ketu Idi 7°11’N, 2°49’E 10 8 80.0 4 Balogun Balogun 7°02’N, 3°01’E 5 2 40.0 5 Agbon Idi 7°02’N, 2°50’E 5 3 60.0 6 Ijoun Yewa 7°08’N, 2°51’E 10 10 100.0 7 Ayetoro Bareke 7°12’N, 3°12’E 34 8 23.5 8 Owode Yewa 7°07’N, 2°53’E 42 8 19.0 9 Igan Alade Yewa 7°03’N, 2°54’E 6 3 50.0 149 52 MATERIAL AND METHODS A total of 149 snails morphologically conforming on its morphological characters according to BROWN to the genus Bulinus were collected between March (1994), and then preserved in 70% ethanol. and May 2013 from five rivers. Human-water contact Genomic DNA was extracted from each snail fol- sites in the rivers were located with the aid of GPS lowing a modified method ofS TOTHARD et al. (1996). (Magellan Explorist 310, MiTAC Digital corpora- Each snail was removed from the 70% ethanol and tion, CA 95050 USA) and were searched for Bulinus. soaked in TE buffer, pH 7.4 (10 mM Tris HCl and 1 Sampling was carried out along the shoreline of each mM EDTA) overnight so as to remove residual eth- contact site using a standard snail scoop net by the anol. Tissue from each snail was placed in a sterile same collector: 30 passes of the net were supple- 1.5-ml microcentrifuge tube, with 500 µl of CTAB mented with manual search for 30 minutes accord- solution (0.2% 2-mercaptoethanol, 2% hexadecyltri- ing to the method of OLOFINTOYE & ODAIBO (1999). methyl-ammonium bromide (CTAB), 100 mM Tris Snails attached to macrophytes were collected man- (hydroxymethyl) amino-methane, 16 mM EDTA, 1.4 ually. The snails were transported to the laboratory M sodium chloride) and the tissue homogenised. in pre-labelled plastic containers, rinsed, sorted and Proteinase K solution (10 µl at 20 mg/ml) was added counted.
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