Transcriptomic profiling of host-parasite interactions in the microsporidian Trachipleistophora hominis
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BACKGROUND: Trachipleistophora hominis was isolated from an HIV/AIDS patient and is a member of a highly successful group of obligate intracellular parasites. METHODS: Here we have investigated the evolution of the parasite and the interplay between host and parasite gene expression using transcriptomics of T. hominis-infected rabbit kidney cells. RESULTS: T. hominis has about 30% more genes than small-genome microsporidians. Highly expressed genes include those involved in growth, replication, defence against oxidative stress, and a large fraction of uncharacterised genes. Chaperones are also highly expressed and may buffer the deleterious effects of the large number of non-synonymous mutations observed in essential T. hominis genes. Host expression suggests a general cellular shutdown upon infection, but ATP, amino sugar and nucleotide sugar production appear enhanced, potentially providing the parasite with substrates it cannot make itself. Expression divergence of duplicated genes, including transporters used to acquire host metabolites, demonstrates ongoing functional diversification during microsporidian evolution. We identified overlapping transcription at more than 100 loci in the sparse T. hominis genome, demonstrating that this feature is not caused by genome compaction. The detection of additional transposons of insect origin strongly suggests that the natural host for T. hominis is an insect. CONCLUSIONS: Our results reveal that the evolution of contemporary microsporidian genomes is highly dynamic and innovative. Moreover, highly expressed T. hominis genes of unknown function include a cohort that are shared among all microsporidians, indicating that some strongly conserved features of the biology of these enormously successful parasites remain uncharacterised.
This work was supported by a BBSRC studentship to A.K.W., a Marie Curie Intra-European postdoctoral fellowship to T.A.W., and the European Research Council Advanced Investigator Programme (ERC- 2010-AdG-268701) and the Wellcome Trust (grant number 045404) to T.M.E. K.A.M. was supported by a Wellcome Trust Institutional Strategic Support Award (WT097835MF) We thank M. E. Geggie and E. Kozhevnikova for assistance with cell culture and lab reagents, Dr. S. E. Campbell for assistance in RNA purification and sample preparation, Dr. K. Moore and A. Farbos at the Exeter Sequencing Service for assistance in Illumina sequencing and library preparation. Dr T. A. Booth for microscopy training and K. Sendra, A. Farbos, and Dr. S. E. Heaps for helpful discussions. We also thank the two anonymous reviewers for their insightful comments.
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Vol. 16, article 983
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