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1 Gut-Associated Bacteria Invade the Midgut Epithelium of Aedes Aegypti And bioRxiv preprint doi: https://doi.org/10.1101/866897; this version posted January 16, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 1 Gut-associated bacteria invade the midgut epithelium of Aedes aegypti and 2 stimulate innate immunity and suppress Zika virus infection in cells. 3 4 Shivanand Hegde1,2, Denis Voronin3, Aitor Casas-Sanchez1,2 Miguel A. Saldaña4, Eva 5 Heinz1,5, Alvaro Acosta-Serrano1,2, Vsevolod L. Popov6, Ashok K. Chopra4, Grant L. 6 Hughes1,2# 7 8 1Department of Vector Biology, Liverpool School of Tropical Medicine, Liverpool, United 9 Kingdom 10 2Department of Tropical Disease Biology, Liverpool School of Tropical Medicine, 11 Liverpool, United Kingdom 12 3Laboratory of Molecular Parasitology, New York Blood Center, New York, NY, USA 13 4Department of Microbiology and Immunology, University of Texas Medical Branch, 14 Galveston, TX, USA. 15 5Department of Clinical Sciences, Liverpool School of Tropical Medicine, Liverpool, 16 United Kingdom. 17 6Department of Pathology, University of Texas Medical Branch, Galveston, TX, USA. 18 #Corresponding author. Grant Hughes: [email protected] 19 20 21 22 1 bioRxiv preprint doi: https://doi.org/10.1101/866897; this version posted January 16, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 23 Abstract 24 Microbiota within mosquitoes influence nutrition, immunity, fecundity, and the capacity 25 to transmit pathogens. Despite their importance, we have a limited understanding of 26 host-microbiota interactions, especially at the cellular level. It is evident bacterial 27 symbionts that are localized within the midgut also infect other organs within the 28 mosquito; however, the route these symbionts take to colonize other tissues is 29 unknown. Here, utilizing the gentamicin protection assay, we showed that the bacterial 30 symbionts Cedecea and Serratia have the capacity to invade and reside intracellularly 31 within mosquito cells. Symbiotic bacteria were found within a vacuole and bacterial 32 replication was observed in mosquito cell by transmission electron microscopy, 33 indicating bacteria were adapted to the intracellular milieu. Using gene silencing, we 34 determined that bacteria exploited host factors, including actin and integrin receptors, to 35 actively invade mosquito cells. As microbiota can affect pathogens within mosquitoes, 36 we examined the influence of intracellular symbionts on Zika virus (ZIKV) infection. 37 Mosquito cells harbouring intracellular bacteria had significantly less ZIKV compared to 38 uninfected cells or cells exposed to non-invasive bacteria. Intracellular bacteria were 39 observed to substantially upregulate the Toll and IMD innate immune pathways, 40 providing a possible mechanism mediating these anti-viral effects. Examining mono- 41 axenically infected mosquitoes using transmission electron and fluorescent microscopy 42 revealed that bacteria occupied an intracellular niche in vivo. Our results provided 43 evidence that bacteria that associate with the midgut of mosquitoes have intracellular 44 lifestyles which likely have implications for mosquito biology and pathogen infection. 45 This study expands our understanding of host-microbiota interactions in mosquitoes, 2 bioRxiv preprint doi: https://doi.org/10.1101/866897; this version posted January 16, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 46 which is important as symbiont microbes are being exploited for vector control 47 strategies. 48 3 bioRxiv preprint doi: https://doi.org/10.1101/866897; this version posted January 16, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 49 Introduction 50 Mosquitoes are holometabolous insects with aquatic and terrestrial life stages. Aquatic 51 stages are continually exposed to microbes in the larval habitat while adults likely 52 acquire microbiota from the environment after eclosion or when nectar feeding [1-3]. 53 Additionally, environmentally acquired microbes may persist in mosquito tissues 54 between aquatic and adult life states facilitating transstadial transmission [4-6]. It is 55 likely that these processes contribute to the considerable variability seen in the adult 56 microbiome [7-9]. While our understanding of genetic factors that influence host- 57 microbe interactions and microbiome acquisition are expanding [10, 11], we still have a 58 poor knowledge of these interactions at the cellular level. Given the importance of the 59 microbiome on mosquito traits relevant for vectorial capacity and vector competence 60 [12-15], understanding processes that influence microbiome homeostasis is critical for 61 developing microbial-based control strategies [16, 17]. 62 63 Bacterial microbiota often resides within several organs in mosquitoes and appears to 64 be able to migrate between tissues. Several studies have identified bacteria in the gut of 65 mosquitoes [9, 18-20], which have led to these microbes being commonly referred to as 66 gut microbes, but many of these bacterial species also colonize other tissues such as 67 the salivary gland [18, 20-23], reproductive tract [20, 22, 24], or malpighian tubules [4]. 68 While some bacteria are unique to each tissue, several infect multiple tissues within the 69 mosquito [20, 25], and localization in organs such as the malpighian tubules and 70 reproductive tissues likely enables transmission between life stages and generations, 71 respectively. Both Asaia and Serratia are transferred vertically to progeny after 4 bioRxiv preprint doi: https://doi.org/10.1101/866897; this version posted January 16, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 72 administered to the mosquito in a sugar meal, suggesting symbiotic bacteria have the 73 capacity to translocate from the midgut to the germline of their host [20, 26-28]. 74 However, mechanisms facilitating their translocation remain elusive. Infection of the 75 entomopathogic fungus Beavaria of Anopheles mosquitoes enabled Serratia to escape 76 the midgut and over replicate in the hemolymph, which was the cause of mortality to the 77 insect [29]. In Drosophila, orally infected Serratia localized within the midgut epithelium 78 [30]. While the epithelial infection was rare in wild type flies, Serratia was observed to 79 localize intracellularly in imd knock-out flies, suggesting that host immunity influenced 80 cellular localization or controlled infections [30]. Although intracellular bacterial 81 infections have been observed in the midgut of flies [30], cellularity of gut-associated 82 bacterial infections in mosquitoes and the mechaimism facilitating systemic infection of 83 different tissues is largely unknown. It is plausible that an intracellular lifestyle could 84 provide a mechanism for transstadial and vertical transmission of bacteria in mosquito 85 vectors. 86 87 In mammalian systems, bacteria exploit their invasive capability to colonize host tissue 88 and systemically spread within multicellular organisms [31-33]. Pathogenic bacteria like 89 Listeria, Salmonella, Vibrio, and Yersinia invade host cells to colonize, replicate, and 90 migrate between cells [32]. While the invasive capacity and mechanisms have been 91 studied extensively in mammalian cells, in vitro investigation in mosquitoes or other 92 arthropod vectors is lacking. In order to obtain a more complete understanding of the 93 cellularity of bacteria associated with mosquitoes, we assessed the invasive capability 94 of two common Enterobacteriaceae bacteria in mosquito cells using the gentamicin 5 bioRxiv preprint doi: https://doi.org/10.1101/866897; this version posted January 16, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 95 invasion assay. Using this in vitro assay, we characterized the invasive process, 96 examined the mechanisms by which bacteria invade cells, and assessed the effect of 97 intracellular bacteria on host immunity and Zika virus (ZIKV) infection. Importantly, using 98 mono-axenically infected mosquitoes, we found that these bacteria have intracellular 99 localization in mosquitoes. This work expands our understanding of host-microbe 100 interactions of gut-associated symbionts in medically relevant mosquito vectors at the 101 cellular level. 102 103 Results and Discussion 104 Symbiotic bacteria invade mosquito cells in vitro 105 Horizontally acquired bacteria are generally considered to infect the gut lumen, they are 106 also found in other organs of mosquitoes including the salivary glands, malpighian 107 tubules, and germline [3, 4, 6, 25, 34]. It remains unknown how these tissues become 108 infected, but it has been proposed these organs may act as a reservoir to facilitate 109 transstadial transmission of microbes between mosquito life stages [4, 5]. One 110 possibility is that gut bacteria exploit their intracellular lifestyle to transition between host 111 tissues. Therefore, we investigated the capacity of bacteria commonly
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