Transcriptomic Analysis of Toxoplasma Development Reveals Many Novel Functions and Structures Specific to Sporozoites and Oocysts
Open Access
- 13 February 2012
- journal article
- research article
- Published by Public Library of Science (PLoS) in PLOS ONE
- Vol. 7 (2), e29998
- https://doi.org/10.1371/journal.pone.0029998
Abstract
Sexual reproduction of Toxoplasma gondii occurs exclusively within enterocytes of the definitive felid host. The resulting immature oocysts are excreted into the environment during defecation, where in the days following, they undergo a complex developmental process. Within each oocyst, this culminates in the generation of two sporocysts, each containing 4 sporozoites. A single felid host is capable of shedding millions of oocysts, which can survive for years in the environment, are resistant to most methods of microbial inactivation during water-treatment and are capable of producing infection in warm-blooded hosts at doses as low as 1–10 ingested oocysts. Despite its extremely interesting developmental biology and crucial role in initiating an infection, almost nothing is known about the oocyst stage beyond morphological descriptions. Here, we present a complete transcriptomic analysis of the oocyst from beginning to end of its development. In addition, and to identify genes whose expression is unique to this developmental form, we compared the transcriptomes of developing oocysts with those of in vitro-derived tachyzoites and in vivo-derived bradyzoites. Our results reveal many genes whose expression is specifically up- or down-regulated in different developmental stages, including many genes that are likely critical to oocyst development, wall formation, resistance to environmental destruction and sporozoite infectivity. Of special note is the up-regulation of genes that appear “off” in tachyzoites and bradyzoites but that encode homologues of proteins known to serve key functions in those asexual stages, including a novel pairing of sporozoite-specific paralogues of AMA1 and RON2, two proteins that have recently been shown to form a crucial bridge during tachyzoite invasion of host cells. This work provides the first in-depth insight into the development and functioning of one of the most important but least studied stages in the Toxoplasma life cycle.Keywords
This publication has 100 references indexed in Scilit:
- Methods to produce and safely work with large numbers of Toxoplasma gondii oocysts and bradyzoite cystsJournal of Microbiological Methods, 2012
- Identification of Tissue Cyst Wall Components by Transcriptome Analysis of In Vivo and In Vitro Toxoplasma gondii BradyzoitesEukaryotic Cell, 2011
- Polymorphic family of injected pseudokinases is paramount in Toxoplasma virulenceProceedings of the National Academy of Sciences of the United States of America, 2011
- Molecular characterisation of a novel family of cysteine-rich proteins of Toxoplasma gondii and ultrastructural evidence of oocyst wall localisationInternational Journal for Parasitology, 2010
- A Cluster of Four Surface Antigen Genes Specifically Expressed in Bradyzoites,SAG2CDXY, Plays an Important Role inToxoplasma gondiiPersistenceInfection and Immunity, 2008
- PbSR is synthesized in macrogametocytes and involved in formation of the malaria crystalloidsMolecular Microbiology, 2008
- Bradyzoite-Specific Surface Antigen SRS9 Plays a Role in Maintaining Toxoplasma gondii Persistence in the Brain and in Host Control of Parasite Replication in the IntestineInfection and Immunity, 2007
- Toxoplasma co-opts host gene expression by injection of a polymorphic kinase homologueNature, 2006
- Polymorphic Secreted Kinases Are Key Virulence Factors in ToxoplasmosisScience, 2006
- Meiosis-Specific DNA Double-Strand Breaks Are Catalyzed by Spo11, a Member of a Widely Conserved Protein FamilyCell, 1997