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Wolbachia Endobacteria in Natural Populations of Culex Pipiens of Iran and Its Phylogenetic Congruence

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Wolbachia Endobacteria in Natural Populations of Culex Pipiens of Iran and Its Phylogenetic Congruence J Arthropod-Borne Dis, September 2016, 10(3): 349–365 M Karami et al.: Wolbachia Endobacteria … Original Article Wolbachia Endobacteria in Natural Populations of Culex pipiens of Iran and its Phylogenetic Congruence Mohsen Karami 1, *Seyed Hassan Moosa-Kazemi 1, *Mohammad Ali Oshaghi 1, Hasan Vatandoost 1, Mohammad Mehdi Sedaghat 1, Ramazan Rajabnia 2, Mostafa Hosseini 3, Naseh Maleki-Ravasan 4, Yousef Yahyapour 2, Elaheh Ferdosi- Shahandashti 5 1Department of Medical Entomology and Vector Control, School of Public Health, Tehran University of Medical Sciences, Tehran, Iran 2Infectious Diseases & Tropical Medicine Research Center, Babol University of Medical Sciences, Babol, Iran 3Department of Epidemiology and Biostatistics, School of Public Health, Tehran University of Medical Sciences, Tehran, Iran 4Malaria and Vector Research Group, Biotechnology Research Center, Pasteur Institute of Iran, Tehran, Iran 5Department of Advanced Technologies in Medicine (SATiM), Medical Biotechnology,Tehran University of Medical Sciences, Tehran, Iran (Apr 2015; accepted 3 Oct 2015 ١٥ Received) Abstract Background: Wolbachia are common intracellular bacteria that infect different groups of arthropods including mos- quitoes. These bacteria modify host biology and may induce feminization, parthenogenesis, male killing and cyto- plasmic incompatibility (CI). Recently Wolbachia is being nominated as a bio-agent and paratransgenic candidate to control mosquito borne diseases. Methods: Here we report the results of a survey for presence, frequency, and phylogenetic congruence of these en- dosymbiont bacteria in Culex pipiens populations in Northern, Central, and Southern parts of Iran using nested-PCR amplification of wsp gene. Results: Wolbachia DNA were found in 227 (87.3%) out of 260 wild-caught mosquitoes. The rate of infection in adult females ranged from 61.5% to 100%, while in males were from 80% to 100%. The Blast search and phyloge- netic analysis of the wsp gene sequence revealed that the Wolbachia strain from Iranian Cx. pipiens was identical to the Wolbachia strains of supergroup B previously reported in members of the Cx. pipiens complex. They had also identical sequence homology with the Wolbachia strains from a group of distinct arthropods including lepidopteran, wasps, flies, damselfly, thrips, and mites from remote geographical areas of the world. Conclusion: It is suggested that Wolbachia strains horizontally transfer between unrelated host organisms over evo- lutionary time. Also results of this study indicates that Wolbachia infections were highly prevalent infecting all Cx. pipiens populations throughout the country, however further study needs to define Wolbachia inter-population repro- ductive incompatibility pattern and its usefulness as a bio-agent control measure. Keywords: Culex pipiens, Wolbachia, cytoplasmic incompatibility, nested-PCR, Iran Introduction Mosquitoes including Culex pipiens com- Nile, St Louis, Sindbis, Wuchereria bancrofti, plex with global distribution are vectors of ar- Dirofilaria immitis, D. repens, Plasmodium boviral pathogens and parasites such as West relictum, and P. gallinaceum (Vinogradova *Corresponding author: Dr Seyed Hassan Moosa- 349 Kazemi, Email: [email protected], Dr Moham- http://jad.tums.ac.ir mad Ali Oshaghi, E-mail: [email protected] Published Online: January 06, 2016 J Arthropod-Borne Dis, September 2016, 10(3): 349–365 M Karami et al.: Wolbachia Endobacteria … 2000, Pawelek et al. 2014). Among the ‘ne- al. 1997), and Anopheles gambiae and An. glected’ mosquito-borne diseases, lymphatic stephensi, two main malaria vectors (Rasgon filariasis continues to be a hazard to over a 2011, Wang and Jacobs-Lorena 2013). These billion people in 83 countries (O'Connor et data showed that the genetically manipulated al. 2012). Culex pipiens is a species complex symbionts could interfere with the develop- and comprise Cx. quinquefasciatus and Cx. ment of the parasites in the vectors and pro- pipiens in South and North America, Asia vide the groundwork for the use of genet- and Africa, as well as Cx. globocoxitus and ically modified symbionts as a potent tool to Cx. australicus in Australia (Farajollahi et al. battle vector borne diseases. 2011). Culex pipiens and Cx. quinquefascia- The bacterium of Wolbachia pipientis is tus are distributed in most parts of Iran rang- an intracellular organism and inherited ma- ing from north to south (Zaim 1986, Azari- ternally. It is established in more than 20% Hamidian 2007, Nikookar et al. 2010, of all insects and a vast majority of other ar- Khoshdel-Nezamiha et al. 2013, Banafshi et thropods as well as filarial nematodes (Wer- al. 2013, Dehghan et al. 2013, 2014). ren 1997a, Dobson 2004, Lo and Evans The raising of resistance to current insec- 2007). Recent studies imply that 20–76% of ticides by insect vectors (Hemingway and investigated insects give shelter to Wolbach- Ranson 2000), the progress of drug re- ia (Hilgenboecker et al. 2008), as well as sistance in parasites (Talisuna et al. 2004) many arachnids, terrestrial crustaceans, and and lack of clinical cures or vaccines for mites (Cordaux et al. 2001, Gotoh et al. many vector borne diseases have led re- 2003, Rowley et al. 2004). This unique en- searchers to develop urgently new and ad- dosymbiont species was originally found in vanced approaches to control of the diseases. Cx pipiens but later molecular studies have Paratransgenesis, as a new approach, direct discovered a number of phylogenetically di- towards reducing vector competence through verse strains within the species (Lo et al. genetically manipulated symbionts (Coutinho- 2007). This endosymbiont bacterium has Abreu et al. 2010). Transformed symbionts significant effects on its arthropod hosts and are distributed across the insect population nominated as a bioagent to control important via transovarial or transstadial transmision arthropod pests. routs (Durvasula et al. 1997, Chavshin et al. Wolbachia is the cause of various modifi- 2012, 2014, 2015, Maleki-Ravasan et al. cations in insect reproductive arrangement, 2015). Symbionts currently aimed at in par- comprising male-killing, feminization, cyto- atransgenesis include fungi (Rasgon 2011), plasmic incompatibility (CI), and partheno- symbiont bacteria of triatomine bugs (Dur- genesis (Werren et al. 2008). When CI oc- vasula et al. 1997, Durvasula et al. 1999, curs, sperm and eggs are not able to produce Durvasula et al. 2008), tsetse flies (Cheng feasible progeny (Werren 1997b, Clark et al. and Aksoy 1999), sandflies (Maleki-Ravasan 2003, Beckmann and Fallon 2013). Infected et al. 2015) and mosquitoes (Favia et al. females relative to uninfected ones, partici- 2007, Chavshin et al. 2014), and densovi- pate more in offspring production, which ruses infecting An. gambiae and Ae. aegypti permit Wolbachia to take up by all of host mosquitoes (Ward et al. 2001, Ren et al. individuals even if it cases fitness costs 2008). Recently, paratransgenesis have been (Field et al. 1999). The bacterium also can successfully employed to reduce vector com- be used as a vector for delivering desirable petence of the triatomine bug, Rhodnius pro- genetic modifications in insect populations lixus, vector of Trypanosoma cruzi, the caus- (Werren 1997b). As reviewed by Werren ative agent of Chagas disease (Durvasula et (1997a), Wolbachia have potential roles in 350 http://jad.tums.ac.ir Published Online: January 06, 2016 J Arthropod-Borne Dis, September 2016, 10(3): 349–365 M Karami et al.: Wolbachia Endobacteria … the rapid speciation of their hosts. Also as a pipiens in various geographical regions across pandemic endosymbiont, Wolbachia can be Iran ranging from north to south. Results of recruited to control of a large number of this study will provide fundamental back- human infectious diseases (Slatko et al. ground for understanding ecology, distribu- 2014). In filarial nematodes comprising Wu- tion, and potential utility of Wolbachia as chereria bancrofti, Brugia malayi, Brugia bio-control agent of Cx. pipiens. timori and Onchocerca volvulus that infect humans, Wolbachia are obligated for proper Materials and Methods development, fertility and survival, whereas in arthropods, although they can affect de- Study areas velopment and reproduction, but are not re- The study was conducted in twelve loca- quired for host survival. So Wolbachia have tions belong to three provinces of Iran, Ma- been a target for drug discovery against fila- zandaran in the North (six locations), Isfahan riasis. In vivo/ vitro experiments indicate in the center (3 locations) and Hormozgan in that antibiotics such as doxycycline and tet- the South (3 locations) of the country (Fig. racycline can kill both adults and immature 1). Live larvae, pupae, and adult mosquitoes nematodes through depletion of Wolbachia were collected from different biotypes in- (Foster et al. 2013, Taylor et al. 2014). It is cluding plane, jungle, riverside, rice field also shown that, Wolbachia spp where natu- and human dwellings. rally infected or artificially introduced into vector population can affect and decrease the Mosquito collection mosquitoes competence carrying of viruses, Adult mosquitoes were collected in hu- such as Yellow Fever, Chikungunya, Den- man dwellings monthly for a period of five gue, West Nile, as well as ones transmitting months (June to late October, 2014) by hand- of the Plasmodium protozoans and filarial catch collection method using mouth aspira- nematodes (Bourtzis et al. 2014). tor. Also live larvae
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