Abstract
BackgroundApicomplexan parasites replicate by varied and unusual processes where the typically eukaryotic expansion of cellular components and chromosome cycle are coordinated with the biosynthesis of parasite-specific structures essential for transmission.Methodology/Principal FindingsHere we describe the global cell cycle transcriptome of the tachyzoite stage of Toxoplasma gondii. In dividing tachyzoites, more than a third of the mRNAs exhibit significant cyclical profiles whose timing correlates with biosynthetic events that unfold during daughter parasite formation. These 2,833 mRNAs have a bimodal organization with peak expression occurring in one of two transcriptional waves that are bounded by the transition into S phase and cell cycle exit following cytokinesis. The G1-subtranscriptome is enriched for genes required for basal biosynthetic and metabolic functions, similar to most eukaryotes, while the S/M-subtranscriptome is characterized by the uniquely apicomplexan requirements of parasite maturation, development of specialized organelles, and egress of infectious daughter cells. Two dozen AP2 transcription factors form a series through the tachyzoite cycle with successive sharp peaks of protein expression in the same timeframes as their mRNA patterns, indicating that the mechanisms responsible for the timing of protein delivery might be mediated by AP2 domains with different promoter recognition specificities.Conclusion/SignificanceUnderlying each of the major events in apicomplexan cell cycles, and many more subordinate actions, are dynamic changes in parasite gene expression. The mechanisms responsible for cyclical gene expression timing are likely crucial to the efficiency of parasite replication and may provide new avenues for interfering with parasite growth.
Highlights
Apicomplexan parasites are important pathogens of humans and domestic animals that cause diseases with widespread impacts on global health
Like the Toxoplasma gondii asexual stages studied here, form daughter cells after each round of chromosome replication. This apicomplexan process differs from the binary fission typical of most eukaryotes in that the daughter parasites form by internal budding within the maternal cell which is consumed by the process
Internal daughter formation was cyclical with budding fractions rising to nearly half the population following thymidine-release before falling to,5% and rising again as parasites progressed through the second S phase (Fig. 1, internal daughters)
Summary
Apicomplexan parasites are important pathogens of humans and domestic animals that cause diseases with widespread impacts on global health. Like the Toxoplasma gondii asexual stages studied here, form daughter cells after each round of chromosome replication (endodyogeny). This apicomplexan process differs from the binary fission typical of most eukaryotes in that the daughter parasites form by internal budding within the maternal cell which is consumed by the process. Other apicomplexans may copy their chromosomes and form multiple nuclei, while delaying cytokinesis until the last round of nuclear division or may wait to package haploid genome units into individual nuclei during the final internal budding of new daughter parasites (e.g. schizogony in Plasmodium or endopolygeny in Sarcocystis, respectively) [7,8]. Apicomplexan parasites replicate by varied and unusual processes where the typically eukaryotic expansion of cellular components and chromosome cycle are coordinated with the biosynthesis of parasite-specific structures essential for transmission
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