Abstract
In this study, we investigated the global gene expression responses of Elizabethkingia anophelis to iron fluxes in the midgut of female Anopheles stephensi mosquitoes fed sucrose or blood, and in iron-poor or iron-rich culture conditions. Of 3,686 transcripts revealed by RNAseq technology, 218 were upregulated while 112 were down-regulated under iron-poor conditions. Hemolysin gene expression was significantly repressed when cells were grown under iron-rich or high temperature (37°C) conditions. Furthermore, hemolysin gene expression was down-regulated after a blood meal, indicating that E. anophelis cells responded to excess iron and its associated physiological stress by limiting iron loading. By contrast, genes encoding respiratory chain proteins were up-regulated under iron-rich conditions, allowing these iron-containing proteins to chelate intracellular free iron. In vivo studies showed that growth of E. anophelis cells increased 3-fold in blood-fed mosquitoes over those in sucrose-fed ones. Deletion of siderophore synthesis genes led to impaired cell growth in both iron-rich and iron-poor media. Mutants showed more susceptibility to H2O2 toxicity and less biofilm formation than did wild-type cells. Mosquitoes with E. anophelis experimentally colonized in their guts produced more eggs than did those treated with erythromycin or left unmanipulated, as controls. Results reveal that E. anophelis bacteria respond to varying iron concentration in the mosquito gut, harvest iron while fending off iron-associated stress, contribute to lysis of red blood cells, and positively influence mosquito host fecundity.
Highlights
Elizabethkingia anophelis is an aerobic, non-fermenting, Gram-negative rod (Kämpfer et al, 2011)
Out of the 3,686 transcribed genes detected in this study (Supplementary Table S1), 330 displayed a significant change, which counted for 9% of total transcripts in E. anophelis (Supplementary Table S2)
Multidimensional scaling analysis of the matrix of up- and down-regulated genes by experimental category of high- or low-iron treatment samples showed that the transcriptomes of the biological replicates in iron-rich samples grouped together while they were well separated from those grown under iron-poor conditions (Supplementary Figure S2)
Summary
Elizabethkingia anophelis is an aerobic, non-fermenting, Gram-negative rod (Kämpfer et al, 2011) It is ubiquitously distributed in diverse natural environments including water, soil, sediment, plants, and animal digestive tracts (Wang et al, 2011; Breurec et al, 2016). E. anophelis infection resulted in high mortality in adult Anopheles when injected through the cuticle into the mosquito hemocoel, exhibiting pathogenesis, but stabilized as nonpathogenic symbionts when fed to the mosquitoes and confined to gut (Akhouayri et al, 2013). The association between bacterial infection in mosquitoes and infection in human beings is not established (Lau et al, 2016)
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