Impact of the Insect Microbiome on Arbovirus Transmission

A special issue of Viruses (ISSN 1999-4915). This special issue belongs to the section "Invertebrate Viruses".

Deadline for manuscript submissions: closed (1 March 2015) | Viewed by 72059

Special Issue Editors


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Departments of Pathology and of Microbiology and Immunology, Center of Biodefense and Emerging Infectious Diseases and Center for Tropical Diseases, University of Texas Medical Branch, Galveston, TX 77555-0609, USA
Interests: Epidemiology of arthropod-borne and other zoonotic viral diseases
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Guest Editor
Arbovirus-Entomology Laboratory, Texas Department of State Health Services, Austin, TX, USA
Interests: mosquitoes; arboviruses; vector surveillance; virus-mosquito interactions; epidemiology of mosquito-borne diseases

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Guest Editor
Department of Pathology, Center for Tropical Diseases, and Institute for Human Infection and Immunity, 301 University Blvd, University of Texas Medical Branch, Galveston, TX 77555, USA
Interests: basic research on evolution and pathogenesis of arthropod-borne viruses; virus–mosquito and virus–host interactions and vaccine development

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Guest Editor
Department of Pathology and Center of Biodefense and Emerging Infectious Diseases, Center for Tropical Diseases, Institute for Human Infection and Immunity, University of Texas Medical Branch, 301 University Blvd., Galveston, TX 77555-0609, USA
Interests: basic research on evolution and pathogenesis of arthropod-borne viruses; quasispecies in transmission dynamics and emergence; and discovery and characterization of novel/new viruses
Special Issues, Collections and Topics in MDPI journals

Special Issue Information

Dear Colleagues,

Recent studies have shown that the microbiome of insects can have important impacts on the infection of mosquitoes and other insects with pathogenic viruses. Microbes from different classes, including bacteria, fungi and viruses can impact the outcome of exposure of insects to arboviruses. In addition, over the past few years, development of new technologies has led to the discovery, identification and characterization of a large number of novel viruses in insects. Many of these viruses are insect-specific viruses that have a widespread geographic distribution and are isolated from a wide range of insect vectors capable of transmitting arthropod-borne viral diseases. Currently little is known about their mode of transmission and maintenance among their insect hosts in nature, their potential effect(s) on the susceptibility and vector competence of their host for viral pathogens of vertebrates (arboviruses) or their impact on their hosts’ behavior, fertility, fecundity and survival. The collection of reviews and original research papers in this special issue is intended to summarize and showcase current research on the impact of the microbiome on the outcome of arbovirus infection.

Please send a title and abstract by 1 May 2014 to the Assistant Editor, Ms. Sarah Shao ([email protected]).

Professor Robert B. Tesh
Dr. Bethany Bolling
Professor Scott C. Weaver
Dr. Nikolaos Vasilakis
Guest Editors

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Keywords

  • vector microbiome
  • arbovirus
  • vector competence

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Published Papers (7 papers)

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Research

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1999 KiB  
Article
Potential for Co-Infection of a Mosquito-Specific Flavivirus, Nhumirim Virus, to Block West Nile Virus Transmission in Mosquitoes
by Silvina Goenaga, Joan L. Kenney, Nisha K. Duggal, Mark Delorey, Gregory D. Ebel, Bo Zhang, Silvana C. Levis, Delia A. Enria and Aaron C. Brault
Viruses 2015, 7(11), 5801-5812; https://doi.org/10.3390/v7112911 - 11 Nov 2015
Cited by 112 | Viewed by 10544
Abstract
Nhumirim virus (NHUV) is an insect-specific virus that phylogenetically affiliates with dual-host mosquito-borne flaviviruses. Previous in vitro co-infection experiments demonstrated prior or concurrent infection of Aedes albopictus C6/36 mosquito cells with NHUV resulted in a 10,000-fold reduction in viral production of West Nile [...] Read more.
Nhumirim virus (NHUV) is an insect-specific virus that phylogenetically affiliates with dual-host mosquito-borne flaviviruses. Previous in vitro co-infection experiments demonstrated prior or concurrent infection of Aedes albopictus C6/36 mosquito cells with NHUV resulted in a 10,000-fold reduction in viral production of West Nile virus (WNV). This interference between WNV and NHUV was observed herein in an additional Ae. albopictus mosquito cell line, C7-10. A WNV 2K peptide (V9M) mutant capable of superinfection with a pre-established WNV infection demonstrated a comparable level of interference from NHUV as the parental WNV strain in C6/36 and C7-10 cells. Culex quinquefasciatus and Culex pipiens mosquitoes intrathoracically inoculated with NHUVandWNV, or solely withWNVas a control, were allowed to extrinsically incubate the viruses up to nine and 14 days, respectively, and transmissibility and replication of WNV was determined. The proportion of Cx. quinquefasciatus mosquitoes capable of transmitting WNV was significantly lower for the WNV/NHUV group than the WNV control at seven and nine days post inoculation (dpi), while no differences were observed in the Cx. pipiens inoculation group. By dpi nine, a 40% reduction in transmissibility in mosquitoes from the dual inoculation group was observed compared to the WNV-only control. These data indicate the potential that infection of some Culex spp. vectors with NHUV could serve as a barrier for efficient transmissibility of flaviviruses associated with human disease. Full article
(This article belongs to the Special Issue Impact of the Insect Microbiome on Arbovirus Transmission)
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2057 KiB  
Article
Exposure to West Nile Virus Increases Bacterial Diversity and Immune Gene Expression in Culex pipiens
by Steven D. Zink, Greta A. Van Slyke, Michael J. Palumbo, Laura D. Kramer and Alexander T. Ciota
Viruses 2015, 7(10), 5619-5631; https://doi.org/10.3390/v7102886 - 27 Oct 2015
Cited by 39 | Viewed by 6744
Abstract
Complex interactions between microbial residents of mosquitoes and arboviruses are likely to influence many aspects of vectorial capacity and could potentially have profound effects on patterns of arbovirus transmission. Such interactions have not been well studied for West Nile virus (WNV; Flaviviridae, Flavivirus [...] Read more.
Complex interactions between microbial residents of mosquitoes and arboviruses are likely to influence many aspects of vectorial capacity and could potentially have profound effects on patterns of arbovirus transmission. Such interactions have not been well studied for West Nile virus (WNV; Flaviviridae, Flavivirus) and Culex spp. mosquitoes. We utilized next-generation sequencing of 16S ribosomal RNA bacterial genes derived from Culex pipiens Linnaeus following WNV exposure and/or infection and compared bacterial populations and broad immune responses to unexposed mosquitoes. Our results demonstrate that WNV infection increases the diversity of bacterial populations and is associated with up-regulation of classical invertebrate immune pathways including RNA interference (RNAi), Toll, and Jak-STAT (Janus kinase-Signal Transducer and Activator of Transcription). In addition, WNV exposure alone, without the establishment of infection, results in similar alterations to microbial and immune signatures, although to a lesser extent. Multiple bacterial genera were found in greater abundance inWNV-exposed and/or infected mosquitoes, yet the most consistent and notable was the genus Serratia. Full article
(This article belongs to the Special Issue Impact of the Insect Microbiome on Arbovirus Transmission)
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855 KiB  
Article
Wolbachia Do Not Induce Reactive Oxygen Species-Dependent Immune Pathway Activation in Aedes albopictus
by Jennifer C. Molloy and Steven P. Sinkins
Viruses 2015, 7(8), 4624-4639; https://doi.org/10.3390/v7082836 - 13 Aug 2015
Cited by 29 | Viewed by 8218
Abstract
Aedes albopictus is a major vector of dengue (DENV) and chikungunya (CHIKV) viruses, causing millions of infections annually. It naturally carries, at high frequency, the intracellular inherited bacterial endosymbiont Wolbachia strains wAlbA and wAlbB; transinfection with the higher-density Wolbachia strain wMel from Drosophila [...] Read more.
Aedes albopictus is a major vector of dengue (DENV) and chikungunya (CHIKV) viruses, causing millions of infections annually. It naturally carries, at high frequency, the intracellular inherited bacterial endosymbiont Wolbachia strains wAlbA and wAlbB; transinfection with the higher-density Wolbachia strain wMel from Drosophila melanogaster led to transmission blocking of both arboviruses. The hypothesis that reactive oxygen species (ROS)-induced immune activation plays a role in arbovirus inhibition in this species was examined. In contrast to previous observations in Ae. aegypti, elevation of ROS levels was not observed in either cell lines or mosquito lines carrying the wild-type Wolbachia or higher-density Drosophila Wolbachia strains. There was also no upregulation of genes controlling innate immune pathways or with antioxidant/ROS-producing functions. These data suggest that ROS-mediated immune activation is not an important component of the viral transmission-blocking phenotype in this species. Full article
(This article belongs to the Special Issue Impact of the Insect Microbiome on Arbovirus Transmission)
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596 KiB  
Article
Facilitation of Rice Stripe Virus Accumulation in the Insect Vector by Himetobi P Virus VP1
by Shuo Li, Shangshu Ge, Xi Wang, Lijuan Sun, Zewen Liu and Yijun Zhou
Viruses 2015, 7(3), 1492-1504; https://doi.org/10.3390/v7031492 - 23 Mar 2015
Cited by 12 | Viewed by 8269
Abstract
The small brown planthopper (SBPH) is the main vector for rice stripe virus (RSV), which causes serious rice stripe disease in East Asia. To characterize the virus-vector interactions, the SBPH cDNA library was screened with RSV ribonucleoprotein (RNP) as bait using a GAL4-based [...] Read more.
The small brown planthopper (SBPH) is the main vector for rice stripe virus (RSV), which causes serious rice stripe disease in East Asia. To characterize the virus-vector interactions, the SBPH cDNA library was screened with RSV ribonucleoprotein (RNP) as bait using a GAL4-based yeast two-hybrid system. The interaction between RSV-RNP and the Himetobi P virus (HiPV, an insect picorna-like virus) VP1 protein was identified. The relationships between HiPV and RSV in SBPH were further investigated, and the results showed that the titer of RSV was commonly higher in single insect that exhibited more VP1 expression. After the VP1 gene was repressed by RNA silencing, the accumulation of RSV decreased significantly in the insect, whereas the virus acquisition ability of SBPH was unaffected, which suggests that HiPV VP1 potentially facilitates the accumulation of RSV in SBPH. Full article
(This article belongs to the Special Issue Impact of the Insect Microbiome on Arbovirus Transmission)
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Review

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1262 KiB  
Review
Insect-Specific Virus Discovery: Significance for the Arbovirus Community
by Bethany G. Bolling, Scott C. Weaver, Robert B. Tesh and Nikos Vasilakis
Viruses 2015, 7(9), 4911-4928; https://doi.org/10.3390/v7092851 - 10 Sep 2015
Cited by 199 | Viewed by 15447
Abstract
Arthropod-borne viruses (arboviruses), especially those transmitted by mosquitoes, are a significant cause of morbidity and mortality in humans and animals worldwide. Recent discoveries indicate that mosquitoes are naturally infected with a wide range of other viruses, many within taxa occupied by arboviruses that [...] Read more.
Arthropod-borne viruses (arboviruses), especially those transmitted by mosquitoes, are a significant cause of morbidity and mortality in humans and animals worldwide. Recent discoveries indicate that mosquitoes are naturally infected with a wide range of other viruses, many within taxa occupied by arboviruses that are considered insect-specific. Over the past ten years there has been a dramatic increase in the literature describing novel insect-specific virus detection in mosquitoes, which has provided new insights about viral diversity and evolution, including that of arboviruses. It has also raised questions about what effects the mosquito virome has on arbovirus transmission. Additionally, the discovery of these new viruses has generated interest in their potential use as biological control agents as well as novel vaccine platforms. The arbovirus community will benefit from the growing database of knowledge concerning these newly described viral endosymbionts, as their impacts will likely be far reaching. Full article
(This article belongs to the Special Issue Impact of the Insect Microbiome on Arbovirus Transmission)
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544 KiB  
Review
The Insect Microbiome Modulates Vector Competence for Arboviruses
by Natapong Jupatanakul, Shuzhen Sim and George Dimopoulos
Viruses 2014, 6(11), 4294-4313; https://doi.org/10.3390/v6114294 - 11 Nov 2014
Cited by 135 | Viewed by 12033
Abstract
Diseases caused by arthropod-borne viruses (arboviruses), such as Dengue, West Nile, and Chikungunya, constitute a major global health burden and are increasing in incidence and geographic range. The natural microbiota of insect vectors influences various aspects of host biology, such as nutrition, reproduction, [...] Read more.
Diseases caused by arthropod-borne viruses (arboviruses), such as Dengue, West Nile, and Chikungunya, constitute a major global health burden and are increasing in incidence and geographic range. The natural microbiota of insect vectors influences various aspects of host biology, such as nutrition, reproduction, metabolism, and immunity, and recent studies have highlighted the ability of insect-associated bacteria to reduce vector competence for arboviruses and other pathogens. This reduction can occur through mechanisms, such as immune response activation, resource competition, or the production of anti-viral molecules. Studying the interactions between insect vectors and their microbiota is an important step toward developing alternative strategies for arbovirus transmission control. Full article
(This article belongs to the Special Issue Impact of the Insect Microbiome on Arbovirus Transmission)

Other

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701 KiB  
Short Communication
Genetic Characterization of Goutanap Virus, a Novel Virus Related to Negeviruses, Cileviruses and Higreviruses
by René Kallies, Anne Kopp, Florian Zirkel, Alejandro Estrada, Thomas R. Gillespie, Christian Drosten and Sandra Junglen
Viruses 2014, 6(11), 4346-4357; https://doi.org/10.3390/v6114346 - 12 Nov 2014
Cited by 56 | Viewed by 8922
Abstract
Pools of mosquitoes collected in Côte d’Ivoire and Mexico were tested for cytopathic effects on the mosquito cell line C6/36. Seven pools induced strong cytopathic effects after one to five days post infection and were further investigated by deep sequencing. The genomes of [...] Read more.
Pools of mosquitoes collected in Côte d’Ivoire and Mexico were tested for cytopathic effects on the mosquito cell line C6/36. Seven pools induced strong cytopathic effects after one to five days post infection and were further investigated by deep sequencing. The genomes of six virus isolates from Côte d’Ivoire showed pairwise nucleotide identities of ~99% among each other and of 56%–60% to Dezidougou virus and Wallerfield virus, two insect-specific viruses belonging to the proposed new taxon Negevirus. The novel virus was tentatively named Goutanap virus. The isolate derived from the Mexican mosquitoes showed 95% pairwise identity to Piura virus and was suggested to be a strain of Piura virus, named C6.7-MX-2008. Phylogenetic inferences based on a concatenated alignment of the methyltransferase, helicase, and RNA-dependent RNA polymerase domains showed that the new taxon Negevirus formed two monophyletic clades, named Nelorpivirus and Sandewavirus after the viruses grouping in these clades. Branch lengths separating these clades were equivalent to those of the related genera Cilevirus, Higrevirus and Blunervirus, as well as to those within the family Virgaviridae. Genetic distances and phylogenetic analyses suggest that Nelorpivirus and Sandewavirus might form taxonomic groups on genus level that may define alone or together with Cilevirus, Higrevirus and Blunervirus a viral family. Full article
(This article belongs to the Special Issue Impact of the Insect Microbiome on Arbovirus Transmission)
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