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Florida Medical Entomology Laboratory

Florida Medical Entomology Laboratory

Dr. Eric Caragata

Eric photo in lab

Eric Caragata

Assistant Professor

Mosquito-Microbe Interactions
e.caragata@ufl.edu

Research Interests

Arboviruses, such as dengue virus and West Nile virus, represent a serious threat to more than half of the world’s population. Their transmission is facilitated by a complex series of molecular interactions with their mosquito host. Characterizing these interactions is a major research priority that will facilitate the development of new tools and techniques to control mosquito-transmitted disease.

However, there is a third player in this story: the mosquito microbiome. There is a diverse array of microorganisms including, bacteria, fungi, algae and insect-specific viruses that can associate with mosquitoes. They primarily reside in the mosquito gut, and form a complex and variable microbial community referred to as the ‘microbiota’, which can influence many aspects of mosquito biology from larval development to egg production.

It has also been well established that the microbiota interacts with the mosquito immune system. And, there is a growing body of evidence demonstrating that the presence of certain microorganisms can actually enhance or limit a mosquito’s potential to harbor and transmit certain medically-important pathogens.

Notable amongst these is Wolbachia pipientis, a bacterial endosymbiont that forms intricate relationships with its hosts, modifying many aspects of their biology, and inhibiting infection with many important arboviruses. Consequently, Wolbachia-infected mosquitoes are currently being used in disease control programs around the world.

Wolbachia and other mosquito-associated microorganisms rely on their host to obtain the nutritional resources they need to survive, and this can greatly perturb host metabolism. Arbovirus infection is also heavily dependent on mosquito nutritional resources, and has been linked to mosquito lipids, insulin signaling, and essential micronutrients, amongst others. These host-microbe metabolic interactions can directly or indirectly influence mosquito immunity and pathogen transmission, but crucially, they remain poorly understood.

My laboratory’s primary research aim is to improve understanding of the relationships between mosquitoes, microorganisms and arboviruses, particularly as they relate to host metabolism and immunity. We will use this information as the basis for developing new mosquito control tools, and optimizing current control approaches

Specific research aims

Characterize the microbiota of mosquitoes in Florida

Florida is a hotspot for mosquito biodiversity in the United States, with 80 species present across the state. This includes major vectors of arboviral disease, both native and invasive, and numerous exotic and understudied mosquito species. In our location at the Florida Medical Entomology Laboratory, we are well situated to study wild populations of these species, and to build an understanding of the microorganisms that associate with them in nature.

My aim is to understand why certain microorganisms associate with certain Floridian mosquito species under different conditions. I am particularly interested in variation in mosquito microbial communities between species, between populations of the same species, and due to environmental factors, including human-driven environmental factors. This research aim will serve as the basis for future projects in the lab, as identifying which microorganisms are associated with different mosquito populations under different conditions is the first step towards a broader goal of elucidating the roles of specific microorganisms in mosquito biology.

Determine how the composition of a mosquito’s diet impacts its microbiome

Mosquito diets in nature can be complex and can vary greatly across different habitats. Mosquito larvae feed on the biological material found in their aquatic habitat, which can include decaying plant and animal matter, and microorganisms. Adult females feed on blood for egg production, and also use nectar as a carbohydrate source, while adult males are restricted to feeding on nectar.

These nutritional sources will each favor the growth of different environmental microorganisms that could be ingested by a mosquito, but will also shape the metabolic environment of mosquito tissues, particularly the gut, where the majority of the microbiota dwell. As different microorganisms have distinct metabolic needs, the bioavailability of key nutritional resources will influence community composition, and potentially moderate the host immune response.

I am interested in identifying key metabolites in the diet of larval and adult mosquitoes that cause certain mosquito-associated bacteria to prosper or struggle. These data will then be used to identify patterns underlying mosquito-microbe and microbe-microbe interactions to elucidate microbial niches in the context of mosquito biology.

Elucidate the role of mosquito metabolism in mosquito-microbe-arbovirus interactions

Mosquitoes possess vast networks of metabolic pathways that help to drive their physiological processes, from blood digestion to egg development. Many of these are also intrinsically linked to their immune system, and therefore play an important role in their response to arboviral infection. Critically, these interactions can be moderated by the presence of microorganisms, including bacteria and fungi.

Recent evidence has highlighted the importance of certain host lipids and micronutrients, like iron, to arboviral infection in mosquitoes. I am interested in building on these data and improving our understanding of metabolic-immune networks that underlie mosquito-microbe-arbovirus interactions. To do so, I plan to activate or suppress key mosquito metabolic pathways, and then gauge the impact on the host, its microbiota and infection with medically-important arboviruses.

Examine plasticity in Wolbachia-host immune interactions under different host metabolic states

Infection with the bacterial endosymbiont Wolbachia occurs naturally in many important mosquito vectors, including the dengue and chikungunya vector, Aedes albopictus, and the West Nile vector, Culex quinquefasciatus. These Wolbachia strains have long-established associations with their hosts, but the relationships are not completely mutualistic. They can have a broad impact on host physiology, and alter host reproductive biology to promote their own propagation. Critically, these native Wolbachia infections can still induce an immune response and parasitize host metabolic resources.

I am interested in understanding more about the role of metabolism in the relationship between native Wolbachia infections and their mosquito hosts. Specifically, how Wolbachia x mosquito immune interactions vary in response to changes to host metabolism, and how this affects host biology and response to arboviral infection.

Data from these experiments will help us to understand plasticity in Wolbachia-host relationships; the extent to which they are capable of mounting a stronger or weaker immune response after a metabolic stimulus. This is directly relevant to the ongoing use of Wolbachia as a mosquito control tool, as Wolbachia-host relationships are hypothesized to become more benign, and more similar to a native Wolbachia infection over time, which may eventually weaken their ability to block arboviral infection.

Eric photo in lab

Eric Caragata

Assistant Professor

Mosquito-Microbe Interactions
e.caragata@ufl.edu

  • Ph.D., Vector Biology, University of Queensland, 2013
  • B.Sci. (Hons), Genetics, University of Queensland, 2008
  • B.BusMan., Business Economics, University of Queensland, 2007
Eric photo in lab

Eric Caragata

Assistant Professor

Mosquito-Microbe Interactions
e.caragata@ufl.edu

  • Caragata EP, Dong S, Dong Y, Simões ML, Tikhe CV, Dimopoulos G. Prospects and Pitfalls: Next-Generation Tools to Control Mosquito-Transmitted Disease. Annu Rev Microbiol. 2020 Sep 8;74:455-475. doi: 10.1146/annurev-micro-011320-025557. PMID: 32905752.
  • Caragata EP, Otero LM, Carlson JS, Borhani Dizaji N, Dimopoulos G. 2020. A Nonlive Preparation of Chromobacterium Panama (Csp_P) Is a Highly Effective Larval Mosquito Biopesticide. Appl Environ Microbiol. May 19;86(11):e00240-20. doi: 10.1128/AEM.00240-20. PMID: 32220845; PMCID: PMC7237781.
  • Caragata EP, Tikhe CV, Dimopoulos G. 2019, Opin. Virol. Curious Entanglements: Interactions between Mosquitoes, their Microbiota, and Arboviruses. 37: 26-36. 
  • Caragata EP#, Rocha MN#, Pereira TN, Mansur SB, Dutra HLC, Moreira LA. Pathogen blocking in Wolbachia-infected Aedes aegypti is not affected by Zika and dengue virus co-infection. PLoS Negl Trop Dis. 13(5):e0007443. #Co-first authorship.
  • Simões ML#,Caragata EP#, Dimopoulos G. 2018. Trends Parasitol. Diverse Host and Restriction Factors Regulate Mosquito-Pathogen Interactions. 34(7):603-616. #Co-first authorship.
  • Gesto JSM, Araki AS, Caragata EP, de Oliveira CD, Martins AJ, Bruno RV & Moreira LA. 2018. In tune with nature: Wolbachia does not impair pre-copula acoustic communication in Aedes aegypti. Parasit Vectors. 22;11(1):109.
  • Dutra HLC, Rodrigues SL, Mansur SB, de Oliveira SP, CaragataEP & Moreira LA. 2017. Development and physiological effects of an artificial diet for Wolbachia-infected Aedes aegypti. Sci Rep. 16;7(1):15687.
  • de Oliveira SP, de Oliveira CD, Sant'Anna MRV, Dutra HLC, CaragataEP & Moreira LA. 2017. Wolbachia infection in Aedes aegypti mosquitoes alters blood meal excretion and delays oviposition without affecting trypsin activity. Insect Biochem Mol Biol. 87:65-74.
  • Silva JBL, Alves DM, Bottino-Rojas V, Pereira TN, Sorgine MHF,Caragata EP & Moreira LA. 2017. Wolbachia and dengue virus infection in the mosquito Aedes fluviatilis (Diptera: Culicidae). PLoS One. 21:12(7): e0181678.
  • Pacidônio EC#,Caragata EP#, Alves DM, Marques JT & Moreira LA. 2017. The impact of Wolbachia infection on the rate of vertical transmission of dengue virus in Brazilian Aedes aegypti. Parasit Vectors. 10(1):296. #Co-first authorship.
  • Dutra HL, Caragata EP, Moreira LA. 2017. The re-emerging arboviral threat: Hidden enemies: The emergence of obscure arboviral diseases, and the potential use of Wolbachia in their control. 2017. 39 (2).
  • Caragata EP, Pais FS, Baton LA, Silva JB, Sorgine MHF & Moreira LA. 2017. The transcriptome of the mosquito Aedes fluviatilis (Diptera: Culicidae), and transcriptional changes associated with its native Wolbachia infection. BMC Genomics. 18(1):6.
  • Caragata EP, Rezende FO, Simoes TC, Moreira LA. 2016. Diet-Induced Nutritional Stress and Pathogen Interference in Wolbachia-Infected Aedes aegypti. PLoS Negl Trop Dis. 10(11):e0005158.
  • Caragata EP, Dutra HLC, O'Neill SL, Moreira LA. 2016. Zika control through the bacterium Wolbachia pipientis. Future Microbiol. 11:1499-1502.
  • Caragata EP, Dutra HLC, Moreira LA. 2016. Inhibition of Zika virus by Wolbachia in Aedes aegypti. Microbial Cell. 3(7), 293-295.
  • Dutra HLC, Rocha MN, Dias FBS, Mansur SB, Caragata EP & Moreira LA. 2016. Wolbachia Blocks Currently Circulating Zika Virus Isolates in Brazilian Aedes aegypti Cell Host Microbe, 19, 771-4.
  • Caragata EP, Dutra HLC & Moreira LA. 2016. Exploiting Intimate Relationships: Controlling Mosquito-Transmitted Disease with Wolbachia. Trends Parasitol. 32, 207-18.
  • Skelton E, Rances E, Frentiu FD, Kusmintarsih ES, Iturbe-Ormaetxe I, Caragata EP, Woolfit M & O'Neill SL. 2016. A Native Wolbachia Endosymbiont Does Not Limit Dengue Virus Infection in the Mosquito Aedes notoscriptus (Diptera: Culicidae). J Med Entomol. 53, 401-8.
  • Dutra HLC, dos Santos LM, Caragata EP, Silva JBL, Villela DA, Maciel-de-Freitas R & Moreira LA. 2015. From lab to field: the influence of urban landscapes on the invasive potential of Wolbachia in Brazilian Aedes aegypti PLoS Negl Trop Dis. 9, e0003689.
  • Caragata EP, Rances, E, O'Neill SL & McGraw EA. 2014. Competition for amino acids between Wolbachia and the mosquito host, Aedes aegypti. Microb Ecol, 67, 205-18.
  • Ye YH, Woolfit M, Huttley GA, Rances E, Caragata EP, Popovici J, O'Neill SL & McGraw EA. 2013. Infection with a Virulent Strain of Wolbachia Disrupts Genome Wide-Patterns of Cytosine Methylation in the Mosquito Aedes aegypti. PLoS One, 8e66482.
  • Caragata EP, Rances E, Hedges LM, Gofton AW, Johnson KN, O'Neill SL & McGraw EA. 2013. Dietary cholesterol modulates pathogen blocking by Wolbachia. PLoS Pathog, 9, e1003459.
  • Caragata EP & Walker T. 2012. Using bacteria to treat diseases. Expert Opin Biol Ther. 12, 701-12.
  • Caragata EP, Poinsignon A, Moreira LA, Johnson PH, Leong YS, Ritchie SA, O'Neill SL & McGraw EA. 2011. Improved accuracy of the transcriptional profiling method of age grading in Aedes aegypti mosquitoes under laboratory and semi-field cage conditions and in the presence of Wolbachia Insect Mol Biol, 20, 215-24.
  • Caragata EP, Real KM, Zalucki MP & McGraw EA. 2011. Wolbachia infection increases recapture rate of field-released Drosophila melanogaster. Symbiosis, 54, 55-60.
  • Evans O, Caragata EP, McMeniman CJ, Woolfit M, Green DC, Williams CR, Franklin, CE, O'Neill SL & McGraw EA. 2009. Increased locomotor activity and metabolism of Aedes aegypti infected with a life-shortening strain of Wolbachia pipientis. J Exp Biol, 212, 1436-41.

Book Chapters:

  • Caragata EP & Moreira LA. 2017. Using an Endosymbiont to Control Mosquito-Transmitted Disease. Chapter 7. The Arthropod Vector: Controller of Disease Transmission. Vol. 1: Vector Microbiome and Innate Immunity of Arthropods. Elsevier Publishing. Eds: Stephen Wikel, Serap Aksoy & George Dimopoulos. ISBN: 9780128053508.
  • Caragata EP & Moreira LA. 2017. Wolbachia: Influence on pathogeny, treatment and control of Arthropod-borne diseases. Chapter 38. Arthropod Borne Diseases. Springer Publishing, Ed: Carlos Brisola Marcondes. ISBN:9783319138831.