Dataset Information

Zika virus and temperature modulate Elizabethkingia anophelis in Aedes albopictus.

ABSTRACT:

Background

Vector-borne pathogens must survive and replicate in the hostile environment of an insect's midgut before successful dissemination. Midgut microbiota interfere with pathogen infection by activating the basal immunity of the mosquito and by synthesizing pathogen-inhibitory metabolites.

Methods

The goal of this study was to assess the influence of Zika virus (ZIKV) infection and increased temperature on Aedes albopictus midgut microbiota. Aedes albopictus were reared at diurnal temperatures of day 28 °C/night 24 °C (L) or day 30 °C/night 26 °C (M). The mosquitoes were given infectious blood meals with 2.0 × 10⁸ PFU/ml ZIKV, and 16S rRNA sequencing was performed on midguts at 7 days post-infectious blood meal exposure.

Results

Our findings demonstrate that Elizabethkingia anophelis albopictus was associated with Ae. albopictus midguts exposed to ZIKV infectious blood meal. We observed a negative correlation between ZIKV and E. anophelis albopictus in the midguts of Ae. albopictus. Supplemental feeding of Ae. albopictus with E. anophelis aegypti and ZIKV resulted in reduced ZIKV infection rates. Reduced viral loads were detected in Vero cells that were sequentially infected with E. anophelis aegypti and ZIKV, dengue virus (DENV), or chikungunya virus (CHIKV).

Conclusions

Our findings demonstrate the influence of ZIKV infection and temperature on the Ae. albopictus microbiome along with a negative correlation between ZIKV and E. anophelis albopictus. Our results have important implications for controlling vector-borne pathogens.

SUBMITTER: Onyango MG

PROVIDER: S-EPMC8588690 | biostudies-literature | 2021 Nov

REPOSITORIES: biostudies-literature

ACCESS DATA

Publications

Zika virus and temperature modulate Elizabethkingia anophelis in Aedes albopictus.

Onyango Maria G MG Lange Rachel R Bialosuknia Sean S Payne Anne A Mathias Nicholas N Kuo Lili L Vigneron Aurelien A Nag Dilip D Kramer Laura D LD Ciota Alexander T AT

Parasites & vectors 20211112 1

<h4>Background</h4>Vector-borne pathogens must survive and replicate in the hostile environment of an insect's midgut before successful dissemination. Midgut microbiota interfere with pathogen infection by activating the basal immunity of the mosquito and by synthesizing pathogen-inhibitory metabolites.<h4>Methods</h4>The goal of this study was to assess the influence of Zika virus (ZIKV) infection and increased temperature on Aedes albopictus midgut microbiota. Aedes albopictus were reared at d ...[more]

PMID: 34772442

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Project description:BackgroundZika virus (ZIKV) emerged in the Pacific Ocean and subsequently caused a dramatic Pan-American epidemic after its first appearance in the Northeast region of Brazil in 2015. The virus is transmitted by Aedes mosquitoes. We evaluated the role of temperature and infectious doses of ZIKV in vector competence of Brazilian populations of Ae. aegypti and Ae. albopictus.Methodology/principal findingsTwo Ae. aegypti (Rio de Janeiro and Natal) and two Ae. albopictus (Rio de Janeiro and Manaus) populations were orally challenged with five viral doses (102 to 106 PFU / ml) of a ZIKV strain (Asian genotype) isolated in Northeastern Brazil, and incubated for 14 and 21 days in temperatures mimicking the spring-summer (28°C) and winter-autumn (22°C) mean values in Brazil. Detection of viral particles in the body, head and saliva samples was done by plaque assays in cell culture for determining the infection, dissemination and transmission rates, respectively. Compared with 28°C, at 22°C, transmission rates were significantly lower for both Ae. aegypti populations, and Ae. albopictus were not able to transmit the virus. Ae. albopictus showed low transmission rates even when challenged with the highest viral dose, while both Ae. aegypti populations presented higher of infection, dissemination and transmission rates than Ae. albopictus. Ae. aegypti showed higher transmission efficiency when taking virus doses of 105 and 106 PFU/mL following incubation at 28°C; both Ae. aegypti and Ae. albopictus were unable to transmit ZIKV with virus doses of 102 and 103 PFU/mL, regardless the incubation temperature.Conclusions/significanceThe ingested viral dose and incubation temperature were significant predictors of the proportion of mosquito's biting becoming infectious. Ae. aegypti and Ae. albopictus have the ability to transmit ZIKV when incubated at 28°C. However Brazilian populations of Ae. aegypti exhibit a much higher transmission potential for ZIKV than Ae. albopictus regardless the combination of infection dose and incubation temperature.

Project description:Dengue is a mosquito-borne disease that has been an epidemic in China for many years. Aedes albopictus is the dominant Aedes mosquito species and the main vector of dengue in China. Epidemiologically, dengue mainly occurs in Guangdong Province; it does not occur or rarely occurs in other areas of mainland China. This distribution may be associated with climate, mosquito density, and other factors in different regions; however, the effect of temperature on the vector competence of Ae. albopictus for dengue viruses (DENV) remains unclear. In this study, Ae. albopictus was orally infected with dengue virus 2 (DENV-2) and reared at constant temperatures (18, 23, 28, and 32°C) and a fluctuating temperature (28-23-18°C). The infection status of the midguts, ovaries, and salivary glands of each mosquito was detected by polymerase chain reaction (PCR) at 0, 5, 10, and 15 days post-infection (dpi). DENV-2 RNA copies from positive tissues were quantified by quantitative real time PCR (qRT-PCR). At 18°C, DENV-2 proliferated slowly in the midgut of Ae. albopictus, and the virus could not spread to the salivary glands. At 23 and 28°C, DENV-2 was detected in the ovaries and salivary glands at 10 dpi. The rates of infection, dissemination, population transmission, and DENV-2 copies at 28°C were higher than those at 23°C at any time point. At 32°C, the extrinsic incubation period (EIP) for DENV-2 in Ae. albopictus was only 5 dpi, and the vector competence was the highest among all the temperatures. Compared with 28°C, at 28-23-18°C, the positive rate and the amount of DENV-2 in the salivary glands were significantly lower. Therefore, temperature is an important factor affecting the vector competence of Ae. albopictus for DENV-2. Within the suitable temperature range, the replication of DENV-2 in Ae. albopictus accelerated, and the EIP was shorter with a higher temperature. Our results provide a guide for vector control and an experimental basis for differences in the spatial distribution of dengue cases.

Project description:Both mosquito species-specific differences and virus strain -specific differences impact vector competence. Previous results in our laboratory with individual populations of N. American mosquitoes support studies suggesting Aedes aegypti are more competent than Ae. albopictus for American Zika virus (ZIKV) strains and demonstrate that U.S. Ae. albopictus have higher competence for an ancestral Asian ZIKV strain. A982V, an amino acid substitution in the NS1 gene acquired prior to the American outbreak, has been shown to increase competence in Ae. aegypti. We hypothesized that variability in the NS1 could therefore contribute to species-specific differences and developed a reverse genetics system based on a 2016 ZIKV isolate from Honduras (ZIKV-WTic) to evaluate the phenotypic correlates of individual amino acid substitutions. In addition to A982V, we evaluated G894A, which was acquired during circulation in the Americas. Reversion of 982 and 894 to ancestral residues increased infectivity, transmissibility and viral loads in Ae. albopictus but had no effect on competence or replication in Ae. aegypti. In addition, while host cell-specific differences in NS1 secretion were measured, with significantly higher secretion in mammalian cells relative to mosquito cells, strain-specific differences in secretion were not detected, despite previous reports. These results demonstrate that individual mutations in NS1 can influence competence in a species-specific manner independent of differences in NS1 secretion and further indicate that ancestral NS1 residues confer increased competence in Ae. albopictus. Lastly, experimental infections of Ifnar1-/- mice demonstrated that these NS1 substitutions can influence viral replication in the host and, specifically, that G894A could represent a compensatory change following a fitness loss from A982V with some viral genetic backgrounds. Together these data suggest a possible role for epistatic interactions in ZIKV fitness in invertebrate and vertebrate hosts and demonstrate that strains with increased transmission potential in U.S. Ae. albopictus could emerge.

Project description:BACKGROUND:Much work has been done in recent years to determine the vector competence of Aedes albopictus (Skuse) for Zika virus (ZIKV). If competent, Ae. albopictus could become an important vector in the spread of ZIKV to areas which until now have been considered safe from the virus. Despite much speculation about Ae. albopictus' competence for ZIKV, there have been, to date, no quantitative syntheses of Ae. albopictus' competence, nor have the potentially confounding differences between studies been addressed. METHODOLOGY/ PRINCIPLE FINDINGS:This study represents a quantitative meta-analysis of the literature surrounding this topic by examining infection rates (IR) and transmission rates (TR) among sample populations of Ae. albopictus at 7 and 14 days post infection (dpi) across 15 journal articles comprising 23 studies. Our analyses examined potentially confounding variables in the studies contained therein, including: geographic origin of viral strain or mosquito population tested, whether sympatry of the tested viral strain and mosquito population was important, and freshness of blood meal. Our results suggest 1) Ae albopictus is a competent vector for ZIKV and 2) that origin of Ae. albopictus population and origin of viral strain had significant effects on the competence of Ae. albopictus to transmit ZIKV. CONCLUSIONS/ SIGNIFICANCE:These results indicate a need to further explore the effects of methodology on vector competence studies and to examine in more detail the geographic variation in the competence of Ae. albopictus for ZIKV as well as the underlying causes of said variation. The ability of Ae. albopictus to carry and transmit ZIKV also points to a need to create new vector control strategies in case of a ZIKV outbreak in an area where Ae. albopictus is prominent. Finally, this study represents a potential template for future meta-analyses in the field of vector competence, where this type of study has been under-utilized despite the abundance of relevant studies.

Dataset Information

Zika virus and temperature modulate Elizabethkingia anophelis in Aedes albopictus.

Background

Methods

Results

Conclusions

Publications

Zika virus and temperature modulate Elizabethkingia anophelis in Aedes albopictus.

Similar Datasets

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