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Wolbachia: Endosymbiont of Onchocercid Nematodes and Their Vectors Ranju Ravindran Santhakumari Manoj1, Maria Stefania Latrofa1, Sara Epis2 and Domenico Otranto1,3*

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Wolbachia: Endosymbiont of Onchocercid Nematodes and Their Vectors Ranju Ravindran Santhakumari Manoj1, Maria Stefania Latrofa1, Sara Epis2 and Domenico Otranto1,3* Manoj et al. Parasites Vectors (2021) 14:245 https://doi.org/10.1186/s13071-021-04742-1 Parasites & Vectors REVIEW Open Access Wolbachia: endosymbiont of onchocercid nematodes and their vectors Ranju Ravindran Santhakumari Manoj1, Maria Stefania Latrofa1, Sara Epis2 and Domenico Otranto1,3* Abstract Background: Wolbachia is an obligate intracellular maternally transmitted, gram-negative bacterium which forms a spectrum of endosymbiotic relationships from parasitism to obligatory mutualism in a wide range of arthropods and onchocercid nematodes, respectively. In arthropods Wolbachia produces reproductive manipulations such as male killing, feminization, parthenogenesis and cytoplasmic incompatibility for its propagation and provides an additional ftness beneft for the host to protect against pathogens, whilst in onchocercid nematodes, apart from the mutual metabolic dependence, this bacterium is involved in moulting, embryogenesis, growth and survival of the host. Methods: This review details the molecular data of Wolbachia and its efect on host biology, immunity, ecology and evolution, reproduction, endosymbiont-based treatment and control strategies exploited for flariasis. Relevant peer- reviewed scientic papers available in various authenticated scientifc data bases were considered while writing the review. Conclusions: The information presented provides an overview on Wolbachia biology and its use in the control and/ or treatment of vectors, onchocercid nematodes and viral diseases of medical and veterinary importance. This ofers the development of new approaches for the control of a variety of vector-borne diseases. Keywords: Wolbachia, Endosymbionts, Onchocercid nematodes, Vector, Treatment, Control Background gram-negative bacterium is also transmitted through the Endosymbiosis is an intimate form of symbiotic asso- host germ line to the next generation [5]. After the ini- ciation in which one organism dwells within the body tial discovery in the reproductive organs of Culex pipiens of another, forming a spectrum of relationships from mosquito by M. Hertig and S. B. Wolbach in 1924 [6], parasitism to obligatory mutualism [1]. Many obligate the description of this bacterium took another 12 more mutual symbiotic associations are based on metabolic years [7]. In the late 1960s and early 1970s, ultrastruc- complementation and strengthen or increment the bio- tural studies on flarial nematodes revealed the presence chemical versatility and pathways of one or both hosts of unusual intracellular bodies in the oocyte hypoder- [2, 3]. Wolbachia is a striking example of this mechanism mis of these worms, which were interpreted as bacteria in both onchocercid nematodes and arthropod vectors [8–10] and later identifed as Wolbachia by Sironi and [4]. Tough many endosymbionts have been observed colleagues [11]. Currently, this endosymbiont has been in arthropod and nematode hosts, Wolbachia is the one reported in around 50% of terrestrial arthropod species which is most widely distributed and explored [4]. Like (i.e. insects, mites, crustaceans, spiders, scorpions, col- the mitochondria organelle, this obligate intracellular lembolans) and in several species of onchocercid nema- todes [12, 13]. Similarly, this bacterium has also been identifed in non-flarial plant nematodes, Radopho- *Correspondence: [email protected] 1 Department of Veterinary Medicine, University of Bari, Valenzano, Italy lus similis [14] and Pratylenchus penetrans of the order Full list of author information is available at the end of the article Tylenchida [15]. In onchocercid nematodes, Wolbachia © The Author(s) 2021. This 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:// creat iveco mmons. org/ licen ses/ by/4. 0/. The Creative Commons Public Domain Dedication waiver (http:// creat iveco mmons. org/ publi cdoma in/ zero/1. 0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Manoj et al. Parasites Vectors (2021) 14:245 Page 2 of 24 has a mutual association in which it is involved in embry- arthropod species such as termites, spiders, mites [32], ogenesis, moulting, growth and survival [16] of the flar- bugs (i.e. Cimex lectularius and Montina sp.) [33] and in iae, and it has been hypothesised that the worm provides human flariae (i.e. Mansonella) [34–36], flariae of black essential aminoacids for bacterial growth [17]. However, bear, (Cercopithiflaria japonica) [12] and that of geckoes in arthropods, the “parasitic side” of Wolbachia prevails, (Madathamugadia hiepei) [37]. Currently, a complete in that this bacterium manipulates the host reproduction genome of Wolbachia from the supergroup F is avail- to increase its own ftness and spread into the host popu- able from the wCle strain of C. lectularius [2] and wMhie lation [18, 19]. Reproductive manipulations exerted by strain of M. hiepei [23]. Wolbachia on its hosts have extensively been investigated In particular, supergroups A and B are the most rep- and include male killing, feminization, parthenogenesis resented among arthropods and it is estimated that the and cytoplasmic incompatibility (CI) [4]. Te efects of common ancestor of both would have diverged approxi- Wolbachia presence on its hosts (i.e. host biology, physi- mately 58–67 million years ago. Tough estimation of ology, immunity, ecology, evolution and reproduction) the origin of Wolbachia is a controversial topic and a have been exploited for the development of promising suitable outgroup for phylogenetic analysis of Wolbachia endosymbiont-based strategies for the treatment of fla- is unavailable, it has been suggested that arthropod and riasis and for the control of important vector-borne dis- onchocercid nematode supergroups diverged around eases of medical and veterinary relevance [4]. Tis review 100 million years ago (i.e. 500 million years after their details Wolbachia’s evolution, molecular identifcation, host) [38, 39]. It is important to note that these estima- interaction with arthropods and nematodes and the tions were based on small samplings. Te presence of development of endosymbiont-based treatment and con- Wolbachia in phylogenetically distant hosts such as trol strategies. nematodes and arthropods suggests that these endosym- bionts experienced some type of horizontal transmission Evolutionary history of Wolbachia during their ancient evolution. For example, a horizon- Wolbachia evolved and adapted to its intracellular life- tal transfer of Wolbachia could have occurred from one style in the context of an evolutionary change that host phylum to the other; alternatively, one of the two included other obligatory intracellular organisms (such phyla could have acquired Wolbachia from a third party as the ancestors of Rickettsia, Ehrlichia, Anaplasma and [39]. Incongruence in phylogenies of Wolbachia and Midichloria) and extended over a hundred million years, their arthropod hosts (e.g. the unnatural occurrence of starting from ancient alphaproteobacteria [20–22]. Wol- identical Wolbachia strains in distantly related species) bachia has a small genome (0.8–1.7 Mbp) with large can also be explained by the horizontal transmission of segments of mobile and repetitive DNA, which is uncom- these endosymbionts [38, 40, 41]. In addition, ecological mon in vertically transmitted (generally from mother to events occurring in the transmission and global distribu- ofspring) organisms [4, 23]. Despite the erosive genomic tion of this bacterium in arthropods include the relation- processes due to host restriction and acquisition main- ship between and amongst hosts, such as in the case of tenance, these repetitive host DNA sequences are sup- parasitism, phoresis [42], predation and cannibalism [43], posed to play a major role in the evolution of Wolbachia blood contact after injury [44], presence in parasitoids [24]. Balance among vertical transmission, host switch- [45] or just sharing of common food substrates [46]. ing, recombination insertion sequences and bacte- Unlike arthropods, phylogenetic congruence of nema- riophage sequences helps in the adaptation and global todes with Wolbachia indicates an obligatory dependent distribution of Wolbachia [4, 22]. Based on their main relationship with the organism, followed by host-para- genetic evolution in a large variety of hosts, Wolbachia site co-evolution and vertical transmission via infected have been classifed in 17 supergroups, designated by the females [34, 39]. Tough the association between Wol- letters A to S [23, 25, 26]. Exceptions are represented by bachia and nematodes has been hypothesised to have supergroup G, which was lately been withdrawn because been acquired as a single event [34, 39], recent genome of the high probability of being the result of a genetic analyses suggest multiple
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