Concurrent transcriptional profiling of Dirofilaria immitis and its Wolbachia endosymbiont throughout the nematode life cycle reveals coordinated gene expression

BMC Genomics

Michelle L Michalski¹  Barton E Slatko²  Andrew R Moorhead³  Jeremy M Foster²  Molly D Riggs³  Christopher C Evans³  Ashley N Luck² 

[1] Department of Biology and Microbiology, University of Wisconsin Oshkosh, Oshkosh, WI 54901, USA;New England Biolabs, Inc., Genome Biology Division, 240 County Road, Ipswich, MA 01938, USA;Department of Infectious Diseases, University of Georgia, College Veterinary Medicine, 501 D. W. Brooks Drive, Athens, GA 30602, USA

关键词: RNA-seq;    Wolbachia;    Endosymbiosis;    Transcriptomics;    Filaria;    Nematode;   

Others  :  1090318
DOI  :  10.1186/1471-2164-15-1041

 received in 2014-08-25, accepted in 2014-11-14,  发布年份 2014

【 摘 要 】

Background

Dirofilaria immitis, or canine heartworm, is a filarial nematode parasite that infects dogs and other mammals worldwide. Current disease control relies on regular administration of anthelmintic preventives, however, relatively poor compliance and evidence of developing drug resistance could warrant alternative measures against D. immitis and related human filarial infections be taken. As with many other filarial nematodes, D. immitis contains Wolbachia, an obligate bacterial endosymbiont thought to be involved in providing certain critical metabolites to the nematode. Correlations between nematode and Wolbachia transcriptomes during development have not been examined. Therefore, we detailed the developmental transcriptome of both D. immitis and its Wolbachia (wDi) in order to gain a better understanding of parasite-endosymbiont interactions throughout the nematode life cycle.

Results

Over 215 million single-end 50 bp reads were generated from total RNA from D. immitis adult males and females, microfilariae (mf) and third and fourth-stage larvae (L3 and L4). We critically evaluated the transcriptomes of the various life cycle stages to reveal sex-biased transcriptional patterns, as well as transcriptional differences between larval stages that may be involved in larval maturation. Hierarchical clustering revealed both D. immitis and wDi transcriptional activity in the L3 stage is clearly distinct from other life cycle stages. Interestingly, a large proportion of both D. immitis and wDi genes display microfilarial-biased transcriptional patterns. Concurrent transcriptome sequencing identified potential molecular interactions between parasite and endosymbiont that are more prominent during certain life cycle stages. In support of metabolite provisioning between filarial nematodes and Wolbachia, the synthesis of the critical metabolite, heme, by wDi appears to be synchronized in a stage-specific manner (mf-specific) with the production of heme-binding proteins in D. immitis.

Conclusions

Our integrated transcriptomic study has highlighted interesting correlations between Wolbachia and D. immitis transcription throughout the life cycle and provided a resource that may be used for the development of novel intervention strategies, not only for the treatment and prevention of D. immitis infections, but of other closely related human parasites as well.

【 授权许可】

   
2014 Luck et al.; licensee BioMed Central Ltd.

【 图 表 】

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