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The Tissue Tropisms and Transstadial Transmission of a Rickettsia

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The Tissue Tropisms and Transstadial Transmission of a Rickettsia bioRxiv preprint doi: https://doi.org/10.1101/2020.06.23.166496; this version posted June 23, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC 4.0 International license. 1 The Tissue Tropisms and Transstadial Transmission of a Rickettsia 2 Endosymbiont in the Highland Midge, Culicoides impunctatus 3 (Diptera: Ceratopogonidae) 4 5 Jack Pilgrim1#, Stefanos Siozios1, Matthew Baylis1,2, Gregory D. D. Hurst1 6 7 1. Institute of Infection, Veterinary and Ecological Sciences, Faculty of Health and 8 Life Sciences, University of Liverpool, Liverpool, U.K. 9 2. Health Protection Research Unit in Emerging and Zoonotic Infections, Liverpool, 10 U.K. 11 12 #Address correspondence to Jack Pilgrim, [email protected] 13 14 Running Title: Tropism of Rickettsia in Culicoides impunctatus 15 16 17 18 19 20 1 bioRxiv preprint doi: https://doi.org/10.1101/2020.06.23.166496; this version posted June 23, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC 4.0 International license. 21 Declarations 22 23 Acknowledgments: We would like to thank Dr. Ewa Chrostek for kindly providing 24 comments on the manuscript. We also thank Charlie Winstanley, Matthew Palmer 25 and Lukasz Lukomski for their support with the collection of midge samples. This 26 work was supported by a BBSRC Doctoral Training Partnership studentship awarded 27 to JP. We acknowledge the Liverpool Centre for Cell Imaging (CCI) for provision of 28 imaging equipment and technical assistance (BB/M012441/1). The processing of 29 samples and electron microscopy imaging was undertaken with assistance from 30 Alison Beckett and the Electron Microscopy Unit (Institute of Translational Medicine; 31 University of Liverpool). Culicoides nubeculosus were provided via a Core Capability 32 BBSRC Grant awarded to Simon Carpenter (The Pirbright Institute) and produced by 33 Eric Denison (BBS/E/I/00001701). 34 35 Author contributions: Field and Laboratory work was undertaken by JP and SS. 36 Analysis and interpretation of the data were undertaken by JP, SS and GH, as well 37 as drafting of the manuscript. GH and MB assisted in the conception and design of 38 the study, in addition to critical revision of the manuscript. 39 40 Conflicts of interest: The authors declare that there are no conflicts of interest. 41 42 2 bioRxiv preprint doi: https://doi.org/10.1101/2020.06.23.166496; this version posted June 23, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC 4.0 International license. 43 Abstract 44 Rickettsia are a group of intracellular bacteria which can manipulate host reproduction 45 and alter sensitivity to natural enemy attack in a diverse range of arthropods. The 46 maintenance of Rickettsia endosymbionts in insect populations can be achieved 47 through both vertical and horizontal transmission routes. For example, the presence 48 of the symbiont in the follicle cells and salivary glands of Bemisia whiteflies allows Belli 49 group Rickettsia transmission via the germline and plants, respectively. However, the 50 transmission routes of other Rickettsia, such as those in the Torix group of the genus, 51 remain underexplored. Through fluorescence in-situ hybridisation (FISH) and 52 transmission electron microscopy (TEM) screening, this study describes the pattern of 53 Torix Rickettsia tissue tropisms in the highland midge, Culicoides impunctatus 54 (Diptera: Ceratopogonidae). Of note is high intensity of infection of the ovarian 55 suspensory ligament, suggestive of a novel germline targeting strategy. Additionally, 56 localisation of the symbiont in tissues of several developmental stages suggests 57 transstadial transmission is a major route of ensuring maintenance of Rickettsia within 58 C. impunctatus populations. Aside from providing insights into transmission strategies, 59 Rickettsia presence in the fat body of larvae indicates potential host fitness and vector 60 capacity impacts to be investigated in the future. 61 62 63 64 65 3 bioRxiv preprint doi: https://doi.org/10.1101/2020.06.23.166496; this version posted June 23, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC 4.0 International license. 66 Importance Statement: Microbial symbionts of disease vectors have garnered recent 67 attention due to their ability to alter vectorial capacity. Their consideration as a means 68 of arbovirus control depends on symbiont vertical transmission which leads to spread 69 of the bacteria through a population. Previous work has identified a Rickettsia 70 symbiont present in several vector species of biting midges (Culicoides spp.), 71 however, symbiont transmission strategies and host effects remain underexplored. In 72 this study, we describe the presence of Rickettsia in the ovarian suspensory ligament 73 and the ovarian epithelial sheath of Culicoides impunctatus. Infection of these organs 74 suggest the connective tissue surrounding developing eggs is important for ensuring 75 vertical transmission of the symbiont in midges and possibly other insects. 76 Additionally, our results indicate Rickettsia localisation in the fat body of Culicoides 77 impunctatus. As viruses spread by midges often replicate in the fat body, this implies 78 possible vector competence effects to be further investigated. 79 80 81 82 83 84 85 86 4 bioRxiv preprint doi: https://doi.org/10.1101/2020.06.23.166496; this version posted June 23, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC 4.0 International license. 87 Introduction 88 89 Heritable microbes of arthropods are important drivers of diverse host phenotypes. 90 For example, both Rickettsia and Wolbachia are associated with reproductive 91 parasitisms which favour the production of female offspring (e.g. male-killing and 92 parthenogenesis) (1–3), whilst also being associated with resistance or tolerance 93 against pathogens (4–6). Specifically, in disease vectors such as mosquitoes, both 94 naturally occurring and artificially introduced symbionts can lead to a “virus-blocking” 95 effect (7–10). These phenotypes, combined with maternal inheritance, drive the 96 symbiont (and its effects on vectorial capacity) into a population and is currently being 97 considered as a means of arbovirus control (11–13). 98 99 Culicoides biting midges (Diptera: Ceratopogonidae) are vectors which transmit 100 economically important pathogens of livestock including bluetongue and 101 Schmallenberg viruses (14). Currently, disease control primarily relies on vaccines 102 which, given the rapid emergence and spread of these viruses, are often not available. 103 Thus, alternate strategies, such as those based on symbionts, are of particular interest 104 for midge-borne pathogens. So far, three endosymbionts have been observed in 105 Culicoides spp.; Wolbachia, Cardinium and Rickettsia (15–18). Of these, symbioses 106 with Rickettsia are the most common, and are present in several midge vector 107 species (17). However, effects of the Rickettsia on the host are yet to be determined. 108 The absence of sex-ratio distortion suggests the lack of a reproductive parasitism, and 109 as some midge populations do not carry Rickettsia at fixation (excluding an obligate 5 bioRxiv preprint doi: https://doi.org/10.1101/2020.06.23.166496; this version posted June 23, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC 4.0 International license. 110 association), this indicates the drive of this endosymbiont might be related to a 111 facultative benefit (e.g. pathogen protection). 112 113 This study focusses on broadening our understanding of the interactions between a 114 Torix group Rickettsia and its host the highland midge, Culicoides impunctatus. The 115 presence of Rickettsia in C. impunctatus oocytes has previously been identified and 116 indicates transovariol transmission (17). However, the route of migration to egg 117 chambers by the symbiont is not clear and the tropisms to other tissues remain 118 unexplored. Vertical transmission of non-obligate symbionts is achieved through 119 diverse modes of germline targeting (19). With certain Wolbachia strains of Drosophila 120 spp., the symbiont localises in the germline stem cell niche continuously throughout 121 development (20–22). For other symbionts, such as Belli and Adalia group Rickettsia, 122 germline localisation follows infection of somatic tissues associated with the germline 123 (e.g. follicle cells and bacteriocytes) (23–25). Intriguingly, Rickettsia also has the 124 unusual ability to infect sperm head nuclei, allowing for paternal inheritance, which can 125 combine with maternal transmission to drive a costly symbiont into the population (26). 126 We therefore aimed to explore Rickettsia localisation in the midge germline and its 127 associated tissues to glean insights into germline targeting mechanisms in this 128 symbiosis. 129 130 Another objective of this project is to generate hypotheses of symbiont function 131 through examining patterns of somatic tissue localisation. For instance, the close 132 association of Blattabacterium with uric acid-containing cells (urocytes) in 133 cockroaches is associated with nitrogen recycling into amino acids (27, 28), whilst the 6 bioRxiv preprint doi: https://doi.org/10.1101/2020.06.23.166496; this version posted June 23, 2020.
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