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Microbial Interactions in the Mosquito Gut Determine Serratia Colonization And bioRxiv preprint doi: https://doi.org/10.1101/2020.04.14.039701; this version posted April 14, 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 The copyright holder for this preprint (which was not certified by peer review) is the author/funder.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 Microbial interactions in the mosquito gut determine Serratia colonization and 2 blood feeding propensity. 3 4 Elena V. Kozlova1*, Shivanand Hegde2*, Christopher M. Roundy3, George Golovko4, 5 Miguel A. Saldaña1,5, Charles E. Hart6, Enyia R Anderson2, Emily A Hornett2,7, Kamil 6 Khanipov4, Vsevolod L. Popov1, Maria Pimenova4, Yiyang Zhou8, Yuriy Fovanov4, Scott 7 C. Weaver3, Andrew L. Routh8, Eva Heinz9, Grant L. Hughes2# 8 9 1Department of Pathology, University of Texas Medical Branch, Galveston, TX, USA. 10 2Departments of Vector Biology and Tropical Disease Biology, Centre for Neglected 11 Tropical Disease, Liverpool School of Tropical Medicine, Liverpool, UK. 12 3World Reference Center for Emerging Viruses and Arboviruses, Institute for Human 13 Infections and Immunity, and Department of Microbiology and Immunology, University 14 of Texas Medical Branch, Galveston, TX, USA, 15 4Department of Pharmacology and Toxicology, Sealy Center for Structural Biology, 16 University of Texas Medical Branch, Galveston, TX, United States. 17 5Department of Paediatrics and Tropical Medicine, Baylor College of Medicine, 18 Houston, TX, United States. 19 6The Institute for Translational Science, University of Texas Medical Branch, Galveston, 20 TX, United States. Institute for Global Health and Translational Science and SUNY 21 Center for Environmental Health and Medicine, SUNY Upstate Medical University, 22 Syracuse, NY, United States. 23 7Institute of Integrative Biology, University of Liverpool, Liverpool, UK. 1 bioRxiv preprint doi: https://doi.org/10.1101/2020.04.14.039701; this version posted April 14, 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 The copyright holder for this preprint (which was not certified by peer review) is the author/funder.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. 24 8Department of Biochemistry and Molecular Biology, University of Texas Medical 25 Branch, Galveston, TX, USA, 26 9Departments of Vector Biology and Clinical Sciences, Liverpool School of Tropical 27 Medicine, Liverpool, UK. 28 29 * These authors contributed equally. 30 #Corresponding author. Grant Hughes: [email protected] 31 2 bioRxiv preprint doi: https://doi.org/10.1101/2020.04.14.039701; this version posted April 14, 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. 32 Abstract. 33 How microbe-microbe interactions dictate microbial complexity in the mosquito gut is 34 unclear. Previously we found that Serratia, a gut symbiont that alters vector competence 35 and is being considered for vector control, poorly colonized Aedes aegypti yet was 36 abundant in Culex quinquefasciatus reared under identical conditions. To investigate 37 the incompatibility between Serratia and Ae. aegypti, we characterized two distinct 38 strains of Serratia marcescens from Cx. quinquefasciatus and examined their ability to 39 infect Ae. aegypti. Both Serratia strains poorly infected Ae. aegypti, but when 40 microbiome homeostasis was disrupted, the prevalence and titers of Serratia were 41 similar to the infection in its native host. Examination of multiple genetically diverse Ae. 42 aegypti lines found microbial interference to S. marcescens was commonplace, 43 however one line of Ae. aegypti was susceptible to infection. Microbiome analysis of 44 resistant and susceptible lines indicated an inverse correlation between 45 Enterobacteriaceae bacteria and Serratia, and experimental co-infections in a 46 gnotobiotic system recapitulated the interference phenotype. Furthermore, we observed 47 an effect on host behaviour; Serratia exposure to Ae. aegypti disrupted their feeding 48 behaviour, and this phenotype was also reliant on interactions with their native 49 microbiota. Our work highlights the complexity of host-microbe interactions and provides 50 evidence that microbial interactions influence mosquito behaviour. 51 52 3 bioRxiv preprint doi: https://doi.org/10.1101/2020.04.14.039701; this version posted April 14, 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. 53 Introduction. 54 Mosquitoes harbour a variety of diverse microbes that profoundly alter host 55 phenotypes1-3. In general, the bacterial microbiome can vary considerably between 56 mosquito species and individuals, but within an individual, it is comprised of relatively 57 few bacterial taxa4,5. It is becoming more apparent that a variety of factors contribute to 58 this variation, but we have a lack of understanding regarding why some taxa are present 59 in a host, yet others are absent. In mosquitoes and other insects, much effort has been 60 undertaken to characterize the infection status of species and populations for specific 61 endosymbiotic bacteria such as Wolbachia6-9, yet few studies have examined the 62 infection prevalence of specific gut-associated bacteria in mosquito vectors. It is evident 63 that several gut-associated bacterial taxa are common between phylogenetically diverse 64 mosquito species4,5, but less attention has been paid to identifying incompatible host- 65 microbe associations and the mechanism(s) behind this incompatibility. 66 67 Microbiome assembly in mosquitoes is influenced by the environment, host and 68 bacterial genetics, and stochastic processes. While the host is instrumental in 69 maintaining microbiome homeostasis10-14, evidence is emerging that bacterial genetics 70 and microbe-microbe interactions also dictate the prevalence and abundance of 71 microbiota15-18. It is clear that the microbiome can influence several important 72 phenotypes in mosquito vectors3,19,20, including the ability to transmit pathogens. 73 Therefore, a greater appreciation of factors that influence colonization of the mosquito 74 gut could assist our understanding of mosquito phenotypes important for vectorial 4 bioRxiv preprint doi: https://doi.org/10.1101/2020.04.14.039701; this version posted April 14, 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. 75 capacity. This will be critical for deploying microbial-based approaches to control 76 mosquito-borne disease21,22. 77 78 Serratia is a ubiquitous genus of gut symbionts that is known to infect a diverse array of 79 insects, including taxa within the Homopteran, Hymenopteran, Dipteran, and 80 Lepidopteran orders23-28. Several medically relevant vectors also harbour this 81 bacterium29-33. In mosquitoes, Serratia appears to broadly infect Culicine and Anopheles 82 mosquitoes34-37, and these infections can have important phenotypic effects including 83 altering the ability of these vectors to transmit pathogens38-42. Intriguingly, after 84 sequencing the microbiome of Culex quinquefasciatus, Ae. albopictus and Ae. aegypti 85 mosquitoes reared under identical conditions within the same insectary, we found a 86 species-specific infection cline in Serratia levels4. Serratia was a dominant member of 87 the microbiota within Cx. quinquefasciatus, infected Ae. albopictus at low levels, and 88 poorly infected or was absent from Ae. aegypti4. We also found that field-collected Ae. 89 aegypti from the Houston region (USA) lacked Serratia4. 90 91 Other studies have found variable results in respect to the prevalence of Serratia in the 92 yellow fever mosquito. Using high throughput 16S rRNA amplicon sequencing, Serratia 93 was found to be absent or at low levels in some Ae. aegypti field populations5,38-41, yet 94 present in others35,42. Culture dependent approaches have also confirmed the presence 95 of Serratia in this mosquito species43-46. The variable nature of infection in the field 96 could be due to the presence or absence of this bacterium in the local aquatic 97 environment; however, this does not explain the infection cline we observed in our 5 bioRxiv preprint doi: https://doi.org/10.1101/2020.04.14.039701; this version posted April 14, 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. 98 insectary when rearing Ae. aegypti given that Cx. quinquefasciatus reared in the same 99 insectary was heavily infected4. The lack of Serratia infection in these lab-reared Ae. 100 aegypti mosquitoes suggests there is a maladaptation between this particular mosquito 101 line and Serratia strains. 102 103 To investigate the incompatibility between Serratia and the yellow fever mosquito, we 104 isolated and characterized two distinct strains of S. marcescens present within the Cx. 105 quinquefasciatus microbiome, and examined their ability to infect Ae. aegypti. We found 106 that both S. marcescens strains poorly infected several Ae. aegypti strains. However, 107 inducing dysbiosis in the native microbiota with antibiotics facilitated infections, 108 suggesting the incompatibility was related to microbe-microbe interactions. In addition to 109 microbial antagonism, we found that infection with these S. marcescens strains 110 disrupted the feeding behaviour of mosquitoes. We further show the phenotypes 111 induced by S. marcescens are driven by interactions
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