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2021.08.30.458191.Full.Pdf bioRxiv preprint doi: https://doi.org/10.1101/2021.08.30.458191; this version posted August 31, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity.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-ND 4.0 International license. 1 Title: Intrinsic variation in the vertically transmitted insect-specific core virome of Aedes aegypti 2 Author names: Coatsworth, H.1,2.3, Bozic, J3,4,5, Carrillo, J.3,6,8, Buckner, E. A.3,4,6, Rivers, A. 3 R.3,7, Dinglasan, R. R.1,2,3, and Mathias, D. K.3,4 4 Author affiliations: 5 1Emerging Pathogens Institute, University of Florida, Gainesville, Florida, USA 6 2Department of Infectious Diseases & Immunology, College of Veterinary Medicine, University 7 of Florida, Gainesville, Florida, USA 8 3CDC Southeastern Center of Excellence in Vector Borne Diseases, Gainesville, Florida, USA 9 4Entomology & Nematology Department, Florida Medical Entomology Laboratory, Institute of 10 Food and Agricultural Sciences, University of Florida, Vero Beach, Florida, USA 11 5Department of Entomology, the Center for Infectious Disease Dynamics, and the Huck 12 Institutes of the Life Sciences, the Pennsylvania State University, University Park, PA, USA. 13 6Manatee County Mosquito Control District, Palmetto, Florida, USA 14 7Genomics and Bioinformatics Research Unit, Agricultural Research Service, United States 15 Department of Agriculture, Gainesville, Florida, USA 16 8Lacerta Therapeutics, Production and Development, Alachua Florida, USA 17 Corresponding Author: D. K. Mathias, University of Florida, [email protected] 18 19 Abstract 20 Since 2009, local outbreaks of dengue (serotypes 1-3) mediated by Aedes aegypti mosquitoes have 21 occurred in the United States, particularly in Florida (FL). In 2016 and 2017, dengue virus serotype 22 4 was found alongside several insect-specific viruses (ISVs) in pools of A. aegypti from sites in 23 Manatee County, FL, in the absence of an index case. Although ISVs have been characterized in 24 A. aegypti globally, the constitution of a core virome in natural populations remains unclear. Using 25 mosquitoes sampled from the same area in 2018, we compared baseline ovary viromes of field 26 (G0) and lab (Orlando) A. aegypti via metagenomic RNA sequencing. Across all samples, virome 27 composition varied by sample type (field- or colony-derived). Four ISVs comprised >97% of virus 28 sequences: a novel partiti-like virus (Partitiviridae), a previously described toti-like virus 29 (Totiviridae), unclassified Riboviria, and four previously described orthomyxo-like viruses 30 (Orthormyxoviridae). Whole or partial genomes for the toti-like virus, partiti-like virus, and one 31 orthomyxo-like virus were assembled and analyzed phylogenetically. Multigenerational 32 maintenance of these ISVs was confirmed orthogonally by RT-PCR in G0 and G7 mosquitoes, 33 indicating vertical transmission as the mechanism for ISV sustentation. This study provides 34 fundamental information regarding ISV ecology, persistence, and variation in A. aegypti in nature. 35 1 of 30 bioRxiv preprint doi: https://doi.org/10.1101/2021.08.30.458191; this version posted August 31, 2021. 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-ND 4.0 International license. 36 37 Introduction 38 Mosquito-borne viral diseases such as dengue, chikungunya, and Zika have spread to new areas, 39 putting over half the world’s population at risk of infection (Weaver 2014, Kraemer et al. 2015). 40 This increase is largely correlated with the global expansion of Aedes aegypti and Aedes 41 albopictus mosquitoes, the primary vectors for these arboviruses (Messina et al. 2019, Brady and 42 Hay 2020). In Florida, USA, both vector species are present, and A. aegypti populations thrive in 43 most of the state’s large population centers due to their urban niche (Britch et al. 2008, Reiskind 44 and Lounibos 2013, Wilke et al. 2019) and widespread insecticide resistance (Estep et al. 2018, 45 Mundis et al. 2020). 46 Autochthonous dengue virus (DENV, serotypes 1-3) infections have occurred in 11 of the last 12 47 years in urban centers in South Florida (CDC 2010, Rey 2014, 48 https://www.cdc.gov/dengue/statistics-maps/index.html), while in 2014 and 2016 outbreaks of 49 chikungunya (Kendrick et al. 2014) and Zika (Likos et al. 2016, Grubaugh et al. 2017), 50 respectively, occurred exclusively in counties with recent permanent population records of A. 51 aegypti (Hahn et al. 2017). Since the re-emergence of DENV in the Florida Keys in 2009, local 52 transmission of at least one serotype has occurred in the state each year except in 2017. 53 Moreover, despite the absence of a local human index case, dengue virus serotype 4 (DENV-4) 54 was detected and fully sequenced alongside numerous insect-specific viruses (ISVs) in the 55 abdomens of A. aegypti adult G0 females from Manatee County, Florida, in 2016 and 2017 56 (Boyles et al. 2020). 57 The ability of a mosquito to transmit DENV (i.e., its vector competence) varies based on external 58 environmental variables, the genetic backgrounds of the vector and virus, and the composition of 59 the mosquito’s microbiome (Tabachnick 2013). The latter is complex and includes ISVs, which 60 can only replicate in the cells of insect hosts (Sang et al. 2003, Nasar et al. 2012, Junglen et al., 61 2017). ISVs are pervasive in both wild-caught and laboratory-reared mosquitoes, and co- 62 infection of ISVs from the same viral family as DENV are known to influence the vector 63 competence of A. aegypti (Bolling et al. 2012, Zhang et al. 2017, Atoni et al. 2019, Baidaliuk et 64 al. 2019, Öhlund et al. 2019). However, most recently discovered ISVs belong to other virus 65 families, and given their pervasiveness, a better understanding of their ecology and impact on 66 mosquito biology is needed. The term “core virome” was recently coined to describe the set of 67 ISVs common to the majority of individuals in a mosquito population (Shi et al. 2019). The term 68 has since been divided into two categories: vertical (passed from mother to offspring) and 69 environmental (acquired from the environment) (Shi et al. 2020). To date, research on Aedes 70 mosquitoes suggests that at the population level core viromes are maintained across 71 developmental stages (Shi et al. 2020) and over short time scales (~ 1 year) (Boyles et al. 2020, 72 Shi et al. 2020). However, it is unknown how well vertical core viromes are sustained over 73 longer periods of time, or the degree to which environmental core viromes are transient. 74 Moreover, most colonies commonly used in arbovirus research have yet to be examined, and 75 these could be useful models to address questions about the impact of core viromes on mosquito 76 biology. 2 of 30 bioRxiv preprint doi: https://doi.org/10.1101/2021.08.30.458191; this version posted August 31, 2021. 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-ND 4.0 International license. 77 To begin filling these gaps in knowledge, we used tissue-specific RNA metagenomics and 78 reverse-transcription PCR to follow up on the previous virome profiles characterized for 79 Floridian A. aegypti (Boyles et al. 2020). Our objectives were to i) define the vertically 80 transmitted core virome in ovary pools from G0 field- and lab-derived A. aegypti, ii) examine the 81 persistence of specific core ISVs over time in ovaries of G7 descendants of field-derived females, 82 iii) assess variability among the sexes for core ISVs maintained in a field-derived colony, and iv) 83 use phylogenetics to investigate evolutionary relationships between core virome members and 84 previously described ISVs. We hypothesized that elements of the vertical core virome would be 85 present in both field- and lab-derived “Orlando” (ORL) strain A. aegypti due to both originating 86 from Florida, but that field-derived samples would have higher ISV diversity due to greater 87 environmental variability. We further predicted that male ISV infection status would mimic that 88 of their female counterparts because of efficient vertical transmission and that A. aegypti ISVs 89 would cluster phylogenetically with ISVs from other mosquito taxa. 90 Results 91 Partiti- and toti-like insect-specific viruses dominate the Aedes aegypti virome 92 To identify core virome ISV members as well as compare field versus lab A. aegypti virome 93 diversity, viral reads from each ovary pool were assigned to their lowest common ancestor 94 (LCA) and summed based on read count. Partitiviridae reads comprised between 50-76% of all 95 viral reads in the field-derived Manatee County (Palmetto, P) samples, while unclassified 96 Riboviria reads made up >57% of the viral reads in the ORL sample and between 5-11% of the P 97 samples (Figure 1). Viral reads aligning best with Atrato partiti-like virus 3 were the most 98 prevalent across all the P samples, making up 70, 72, 51, 67 and 76 % of the viral reads (P1 – 5 99 ovary pools respectively), but were completely absent from the ORL sample. Reads aligning to 100 A. aegypti toti-like virus accounted for 19, 17, 33, 10, and 11% of the reads for the P samples, 101 and represented 42% of the ORL sequences. Together, 75-90% of all viral reads from field- 102 derived samples aligned to these two groups (Partitiviridae and Totiviridae).
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