Differential Locus Expansion Distinguishes Toxoplasmatinae Species and Closely Related Strains of Toxoplasma gondii

ABSTRACT Toxoplasma gondii is a human obligate intracellular parasite that has infected over 20% of the world population and has a vast intermediate host range compared to those of its nearest relatives Neospora caninum and Hammondia hammondi. While these 3 species have highly syntenic genomes (80 to 99%), in this study we examined and compared species-specific structural variations, specifically at loci that have undergone local (i.e., tandem) duplication and expansion. To do so, we used genomic sequence coverage analysis to identify and curate T. gondii and N. caninum loci that have undergone duplication and expansion (expanded loci [ELs]). The 53 T. gondii ELs are significantly enriched for genes with predicted signal sequences and single-exon genes and genes that are developmentally regulated at the transcriptional level. We validated 24 T. gondii ELs using comparative genomic hybridization; these data suggested significant copy number variation at these loci. High-molecular-weight Southern blotting for 3 T. gondii ELs revealed that copy number varies across T. gondii lineages and also between members of the same clonal lineage. Using similar methods, we identified 64 N. caninum ELs which were significantly enriched genes belonging to the SAG-related surface (SRS) antigen family. Moreover, there is significantly less overlap (30%) between the expanded gene sets in T. gondii and N. caninum than would be predicted by overall genomic synteny (81%). Consistent with this finding, only 59% of queried T. gondii ELs are similarly duplicated/expanded in H. hammondi despite over 99% genomic synteny between these species. IMPORTANCE Gene duplication, expansion, and diversification are a basis for phenotypic differences both within and between species. This study represents the first characterization of both the extent and degree of overlap in gene duplication and locus expansion across multiple apicomplexan parasite species. The most important finding of this study is that the locus duplications/expansions are quantitatively and qualitatively distinct, despite the high degree of genetic relatedness between the species. Given that these differential expansions are prominent species-specific genetic differences, they may also contribute to some of the more striking phenotypic differences between these species. More broadly, this work is important in providing further support for the idea that postspeciation selection events may have a dramatic impact on locus structure and copy number that overshadows selection on single-copy genes.

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Importance of serological cross-reactivity amongToxoplasma gondii, Hammondiaspp.,Neosporaspp.,Sarcocystisspp. andBesnoitia besnoiti

Parasitology ◽

10.1017/s0031182017000063 ◽

2017 ◽

Vol 144 (7) ◽

pp. 851-868 ◽

Cited By ~ 20

Author(s):

LUÍS F. P. GONDIM ◽

JOSÉ R. MINEO ◽

GEREON SCHARES

Keyword(s):

Toxoplasma Gondii ◽

Neospora Caninum ◽

Cross Reactivity ◽

Besnoitia Besnoiti ◽

Cross Reactions ◽

Epidemiological Surveys ◽

Specific Proteins ◽

Specific Antigens ◽

Species Specific

SUMMARYToxoplasma gondii, Neosporaspp.,Sarcocystisspp.,Hammondiaspp. andBesnoitia besnoitiare genetically related cyst-forming coccidia. Serology is frequently used for the identification ofT. gondii, Neosporaspp. andB. besnoiti-exposed individuals. Serologic cross-reactions occur in different tests among animals infected withT. gondiiandH. hammondi,as well as among animals infected byT. gondiiandN. caninum. Infections caused byN. caninumandN. hughesiare almost indistinguishable by serology.Neospora caninum, B. besnoitiandSarcocystisspp. infections in cattle show some degree of serologic cross-reactivity. Antibody cross-reactivity betweenNeosporaspp. andH. heydorni-infected animals is suspected, but not proven to occur. We review serologic cross-reactivity among animals and/or humans infected withT. gondii, Neosporaspp.,Sarcocystisspp.,Hammondiaspp. andB. besnoiti. Emphasis is laid upon antigens and serological methods forN. caninumdiagnosis which were tested for cross-reactivity with related protozoa. Species-specific antigens, as well as stage-specific proteins have been identified in some of these parasites and have promising use for diagnosis and epidemiological surveys.

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Immediate Interferon Gamma Induction Determines Murine Host Compatibility Differences between Toxoplasma gondii and Neospora caninum

Infection and Immunity ◽

10.1128/iai.00027-20 ◽

2020 ◽

Vol 88 (4) ◽

Cited By ~ 1

Author(s):

Rachel S. Coombs ◽

Matthew L. Blank ◽

Elizabeth D. English ◽

Yaw Adomako-Ankomah ◽

Ifeanyi-Chukwu Samuel Urama ◽

...

Keyword(s):

Toxoplasma Gondii ◽

Immune Responses ◽

Interferon Gamma ◽

Neospora Caninum ◽

Ectopic Expression ◽

Parasite Burden ◽

Interleukin 12 ◽

Content Type ◽

Ifn Γ ◽

And Control

ABSTRACT Rodents are critical for the transmission of Toxoplasma gondii to the definitive feline host via predation, and this relationship has been extensively studied as a model for immune responses to parasites. Neospora caninum is a closely related coccidian parasite of ruminants and canines but is not naturally transmitted by rodents. We compared mouse innate immune responses to N. caninum and T. gondii and found marked differences in cytokine levels and parasite growth kinetics during the first 24 h postinfection (hpi). N. caninum-infected mice produced significantly higher levels of interleukin-12 (IL-12) and interferon gamma (IFN-γ) by as early as 4 hpi, but the level of IFN-γ was significantly lower or undetectable in T. gondii-infected mice during the first 24 hpi. “Immediate” IFN-γ and IL-12p40 production was not detected in MyD88−/− mice. However, unlike IL-12p40−/− and IFN-γ−/− mice, MyD88−/− mice survived N. caninum infections at the dose used in this study. Serial measures of parasite burden showed that MyD88−/− mice were more susceptible to N. caninum infections than wild-type (WT) mice, and control of parasite burdens correlated with a pulse of serum IFN-γ at 3 to 4 days postinfection in the absence of detectable IL-12. Immediate IFN-γ was partially dependent on the T. gondii mouse profilin receptor Toll-like receptor 11 (TLR11), but the ectopic expression of N. caninum profilin in T. gondii had no impact on early IFN-γ production or parasite proliferation. Our data indicate that T. gondii is capable of evading host detection during the first hours after infection, while N. caninum is not, and this is likely due to the early MyD88-dependent recognition of ligands other than profilin.

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Differential Gamma Interferon- and Tumor Necrosis Factor Alpha-Driven Cytokine Response Distinguishes Acute Infection of a Metatherian Host with Toxoplasma gondii and Neospora caninum

Infection and Immunity ◽

10.1128/iai.00173-17 ◽

2017 ◽

Vol 85 (6) ◽

Cited By ~ 7

Author(s):

Shannon L. Donahoe ◽

David N. Phalen ◽

Bronwyn M. McAllan ◽

Denis O'Meally ◽

Milton M. McAllister ◽

...

Keyword(s):

Immune Response ◽

Toxoplasma Gondii ◽

Tumor Necrosis Factor ◽

Tumor Necrosis Factor Alpha ◽

Tumor Necrosis ◽

Neospora Caninum ◽

Necrosis Factor Alpha ◽

Content Type ◽

Factor Alpha ◽

Necrosis Factor

ABSTRACT Toxoplasma gondii and Neospora caninum (both Apicomplexa) are closely related cyst-forming coccidian parasites that differ significantly in their host ranges and ability to cause disease. Unlike eutherian mammals, Australian marsupials (metatherian mammals) have long been thought to be highly susceptible to toxoplasmosis and neosporosis because of their historical isolation from the parasites. In this study, the carnivorous fat-tailed dunnart (Sminthopsis crassicaudata) was used as a disease model to investigate the immune response and susceptibility to infection of an Australian marsupial to T. gondii and N. caninum. The disease outcome was more severe in N. caninum-infected dunnarts than in T. gondii-infected dunnarts, as shown by the severity of clinical and histopathological features of disease and higher tissue parasite burdens in the tissues evaluated. Transcriptome sequencing (RNA-seq) of spleens from infected dunnarts and mitogen-stimulated dunnart splenocytes was used to define the cytokine repertoires. Changes in mRNA expression during the time course of infection were measured using quantitative reverse transcription-PCR (qRT-PCR) for key Th1 (gamma interferon [IFN-γ] and tumor necrosis factor alpha [TNF-α]), Th2 (interleukin 4 [IL-4] and IL-6), and Th17 (IL-17A) cytokines. The results show qualitative differences in cytokine responses by the fat-tailed dunnart to infection with N. caninum and T. gondii. Dunnarts infected with T. gondii were capable of mounting a more effective Th1 immune response than those infected with N. caninum, indicating the role of the immune response in the outcome scenarios of parasite infection in this marsupial mammal.

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In VitroEffects of Novel Ruthenium Complexes in Neospora caninum and Toxoplasma gondii Tachyzoites

Antimicrobial Agents and Chemotherapy ◽

10.1128/aac.02446-12 ◽

2013 ◽

Vol 57 (11) ◽

pp. 5747-5754 ◽

Cited By ~ 19

Author(s):

Fabienne Barna ◽

Karim Debache ◽

Carsten A. Vock ◽

Tatiana Küster ◽

Andrew Hemphill

Keyword(s):

Electron Microscopy ◽

Transmission Electron Microscopy ◽

Toxoplasma Gondii ◽

Neospora Caninum ◽

Ruthenium Complexes ◽

Term Treatment ◽

Content Type ◽

Transmission Electron ◽

Long Term Treatment

ABSTRACTUpon the screening of 16 antiproliferative compounds againstToxoplasma gondiiandNeospora caninum, two hydrolytically stable ruthenium complexes (compounds 16 and 18) exhibited 50% inhibitory concentrations of 18.7 and 41.1 nM (T. gondii) and 6.7 and 11.3 nM (N. caninum). To achieve parasiticidal activity with compound 16, long-term treatment (22 to 27 days at 80 to 160 nM) was required. Transmission electron microscopy demonstrated the rapid impact on and ultrastructural alterations in both parasites. These preliminary findings suggest that the potential of ruthenium-based compounds should thus be further exploited.

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Magnetosome Gene Duplication as an Important Driver in the Evolution of Magnetotaxis in the Alphaproteobacteria

mSystems ◽

10.1128/msystems.00315-19 ◽

2019 ◽

Vol 4 (5) ◽

Cited By ~ 2

Author(s):

Haijian Du ◽

Wenyan Zhang ◽

Wensi Zhang ◽

Weijia Zhang ◽

Hongmiao Pan ◽

...

Keyword(s):

Gene Duplication ◽

Gene Cluster ◽

Geomagnetic Field ◽

Evolutionary Biology ◽

Genomic Analysis ◽

Magnetotactic Bacteria ◽

Duplication Event ◽

Comparative Genomic ◽

Content Type ◽

Evolutionary Trajectories

ABSTRACT The evolution of microbial magnetoreception (or magnetotaxis) is of great interest in the fields of microbiology, evolutionary biology, biophysics, geomicrobiology, and geochemistry. Current genomic data from magnetotactic bacteria (MTB), the only prokaryotes known to be capable of sensing the Earth’s geomagnetic field, suggests an ancient origin of magnetotaxis in the domain Bacteria. Vertical inheritance, followed by multiple independent magnetosome gene cluster loss, is considered to be one of the major forces that drove the evolution of magnetotaxis at or above the class or phylum level, although the evolutionary trajectories at lower taxonomic ranks (e.g., within the class level) remain largely unstudied. Here we report the isolation, cultivation, and sequencing of a novel magnetotactic spirillum belonging to the genus Terasakiella (Terasakiella sp. strain SH-1) within the class Alphaproteobacteria. The complete genome sequence of Terasakiella sp. strain SH-1 revealed an unexpected duplication event of magnetosome genes within the mamAB operon, a group of genes essential for magnetosome biomineralization and magnetotaxis. Intriguingly, further comparative genomic analysis suggests that the duplication of mamAB genes is a common feature in the genomes of alphaproteobacterial MTB. Taken together, with the additional finding that gene duplication appears to have also occurred in some magnetotactic members of the Deltaproteobacteria, our results indicate that gene duplication plays an important role in the evolution of magnetotaxis in the Alphaproteobacteria and perhaps the domain Bacteria. IMPORTANCE A diversity of organisms can sense the geomagnetic field for the purpose of navigation. Magnetotactic bacteria are the most primitive magnetism-sensing organisms known thus far and represent an excellent model system for the study of the origin, evolution, and mechanism of microbial magnetoreception (or magnetotaxis). The present study is the first report focused on magnetosome gene cluster duplication in the Alphaproteobacteria, which suggests the important role of gene duplication in the evolution of magnetotaxis in the Alphaproteobacteria and perhaps the domain Bacteria. A novel scenario for the evolution of magnetotaxis in the Alphaproteobacteria is proposed and may provide new insights into evolution of magnetoreception of higher species.

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A Comparison of Stage Conversion in the Coccidian Apicomplexans Toxoplasma gondii, Hammondia hammondi, and Neospora caninum

Frontiers in Cellular and Infection Microbiology ◽

10.3389/fcimb.2020.608283 ◽

2020 ◽

Vol 10 ◽

Author(s):

Sarah L. Sokol-Borrelli ◽

Rachel S. Coombs ◽

Jon P. Boyle

Keyword(s):

Life Cycle ◽

Toxoplasma Gondii ◽

Stress Responses ◽

Neospora Caninum ◽

Life Forms ◽

New Host ◽

Environmental Signals ◽

Stage Conversion ◽

Genetic Components ◽

Species Specific

Stage conversion is a critical life cycle feature for several Apicomplexan parasites as the ability to switch between life forms is critical for replication, dissemination, pathogenesis and ultimately, transmission to a new host. In order for these developmental transitions to occur, the parasite must first sense changes in their environment, such as the presence of stressors or other environmental signals, and then respond to these signals by initiating global alterations in gene expression. As our understanding of the genetic components required for stage conversion continues to broaden, we can better understand the conserved mechanisms for this process and unique components and their contribution to pathogenesis by comparing stage conversion in multiple closely related species. In this review, we will discuss what is currently known about the mechanisms driving stage conversion in Toxoplasma gondii and its closest relatives Hammondia hammondi and Neospora caninum. Work by us and others has shown that these species have some important differences in the way that they (1) progress through their life cycle and (2) respond to stage conversion initiating stressors. To provide a specific example of species-specific complexities associated with stage conversion, we will discuss our recent published and unpublished work comparing stress responses in T. gondii and H. hammondi.

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Comparative genomic hybridization analysis of craniopharyngiomas

Journal of Neurosurgery ◽

10.3171/jns.2003.98.1.0162 ◽

2003 ◽

Vol 98 (1) ◽

pp. 162-164 ◽

Cited By ~ 24

Author(s):

Shlomit Rienstein ◽

Eric F. Adams ◽

David Pilzer ◽

Ayala Aviram Goldring ◽

Boleslaw Goldman ◽

...

Keyword(s):

Comparative Genomic Hybridization ◽

Copy Number ◽

Molecular Mechanisms ◽

Genetic Alterations ◽

Genomic Alteration ◽

Comparative Genomic ◽

Genomic Hybridization ◽

Dna Copy Number ◽

Content Type ◽

Fine Print

Object. Craniopharyngioma is the most common childhood brain tumor and is thought to arise from embryonic remnants of the Rathke pouch. Some craniopharyngiomas are monoclonal in origin and hence presumably harbor somatic genetic alterations, although the precise molecular mechanisms involved in craniopharyngioma development are unknown. The goal of this study was to identify genetic alterations in craniopharyngiomas. Methods. To gain insight into the molecular mechanisms involved in development of these tumors, the authors analyzed nine adamantinomatous craniopharyngiomas by using comparative genomic hybridization. Six tumors (67%) displayed at least one genomic alteration, and three had six or more alterations. Only two tumors displayed a decrease in DNA copy number, and in all others an increase in DNA copy number was noted. Conclusions. The authors conclude that a subset of craniopharyngiomas consists of monoclonal tumors arising from activation of oncogenes located at specific chromosomal loci.

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Comparative Genomic Analysis Reveals the Distribution, Organization, and Evolution of Metal Resistance Genes in the GenusAcidithiobacillus

Applied and Environmental Microbiology ◽

10.1128/aem.02153-18 ◽

2018 ◽

Vol 85 (2) ◽

Cited By ~ 2

Author(s):

Liangzhi Li ◽

Zhenghua Liu ◽

Delong Meng ◽

Xueduan Liu ◽

Xing Li ◽

...

Keyword(s):

Gene Duplication ◽

Resistance Genes ◽

Evolutionary History ◽

Genomic Analysis ◽

Purifying Selection ◽

Metal Resistance ◽

Comparative Genomic Analysis ◽

Comparative Genomic ◽

Content Type ◽

History Of

ABSTRACTMembers of the genusAcidithiobacillus, which can adapt to extremely high concentrations of heavy metals, are universally found at acid mine drainage (AMD) sites. Here, we performed a comparative genomic analysis of 37 strains within the genusAcidithiobacillusto answer the untouched questions as to the mechanisms and the evolutionary history of metal resistance genes inAcidithiobacillusspp. The results showed that the evolutionary history of metal resistance genes inAcidithiobacillusspp. involved a combination of gene gains and losses, horizontal gene transfer (HGT), and gene duplication. Phylogenetic analyses revealed that metal resistance genes inAcidithiobacillusspp. were acquired by early HGT events from species that shared habitats withAcidithiobacillusspp., such asAcidihalobacter,Thiobacillus,Acidiferrobacter, andThiomonasspecies. Multicopper oxidase genes involved in copper detoxification were lost in iron-oxidizingAcidithiobacillus ferridurans,Acidithiobacillus ferrivorans, andAcidithiobacillus ferrooxidansand were replaced by rusticyanin genes during evolution. In addition, widespread purifying selection and the predicted high expression levels emphasized the indispensable roles of metal resistance genes in the ability ofAcidithiobacillusspp. to adapt to harsh environments. Altogether, the results suggested thatAcidithiobacillusspp. recruited and consolidated additional novel functionalities during the adaption to challenging environments via HGT, gene duplication, and purifying selection. This study sheds light on the distribution, organization, functionality, and complex evolutionary history of metal resistance genes inAcidithiobacillusspp.IMPORTANCEHorizontal gene transfer (HGT), natural selection, and gene duplication are three main engines that drive the adaptive evolution of microbial genomes. Previous studies indicated that HGT was a main adaptive mechanism in acidophiles to cope with heavy-metal-rich environments. However, evidences of HGT inAcidithiobacillusspecies in response to challenging metal-rich environments and the mechanisms addressing how metal resistance genes originated and evolved inAcidithiobacillusare still lacking. The findings of this study revealed a fascinating phenomenon of putative cross-phylum HGT, suggesting thatAcidithiobacillusspp. recruited and consolidated additional novel functionalities during the adaption to challenging environments via HGT, gene duplication, and purifying selection. Altogether, the insights gained in this study have improved our understanding of the metal resistance strategies ofAcidithiobacillusspp.

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Integrated Bioinformatic and Targeted Deletion Analyses of the SRS Gene Superfamily Identify SRS29C as a Negative Regulator of Toxoplasma Virulence

mBio ◽

10.1128/mbio.00321-12 ◽

2012 ◽

Vol 3 (6) ◽

Cited By ~ 43

Author(s):

James D. Wasmuth ◽

Viviana Pszenny ◽

Simon Haile ◽

Emily M. Jansen ◽

Alexandra T. Gast ◽

...

Keyword(s):

Toxoplasma Gondii ◽

Gene Deletion ◽

Gene Families ◽

Host Immunity ◽

Negative Regulator ◽

Host Cells ◽

Experimental Investigations ◽

Comparative Genomic ◽

Surface Coat ◽

Content Type

ABSTRACTTheToxoplasma gondiiSRSgene superfamily is structurally related toSRS29B(formerlySAG1), a surface adhesin that binds host cells and stimulates host immunity. Comparative genomic analyses of threeToxoplasmastrains identified 182SRSgenes distributed across 14 chromosomes at 57 genomic loci. Eight distinctSRSsubfamilies were resolved. A core 69 functional gene orthologs were identified, and strain-specific expansions and pseudogenization were common. Gene expression profiling demonstrated differential expression ofSRSgenes in a developmental-stage- and strain-specific fashion and identified nineSRSgenes as priority targets for gene deletion among the tissue-encysting coccidia. A Δsag1 ∆sag2Amutant was significantly attenuated in murine acute virulence and showed upregulated SRS29C (formerly SRS2) expression. Transgenic overexpression of SRS29C in the virulent RH parent was similarly attenuated. Together, these findings reveal SRS29C to be an important regulator of acute virulence in mice and demonstrate the power of integrated genomic analysis to guide experimental investigations.IMPORTANCEParasitic species employ large gene families to subvert host immunity to enable pathogen colonization and cause disease.Toxoplasma gondiicontains a large surface coat gene superfamily that encodes adhesins and virulence factors that facilitate infection in susceptible hosts. We generated an integrated bioinformatic resource to predict which genes from within this 182-gene superfamily of adhesin-encoding genes play an essential role in the host-pathogen interaction. Targeted gene deletion experiments with predicted candidate surface antigens identified SRS29C as an important negative regulator of acute virulence in murine models ofToxoplasmainfection. Our integrated computational and experimental approach provides a comprehensive framework, or road map, for the assembly and discovery of additional key pathogenesis genes contained within other large surface coat gene superfamilies from a broad array of eukaryotic pathogens.

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TgATAT-Mediated α-Tubulin Acetylation Is Required for Division of the Protozoan Parasite Toxoplasma gondii

mSphere ◽

10.1128/msphere.00088-15 ◽

2016 ◽

Vol 1 (1) ◽

Cited By ~ 4

Author(s):

Joseph M. Varberg ◽

Leah R. Padgett ◽

Gustavo Arrizabalaga ◽

William J. Sullivan

Keyword(s):

Toxoplasma Gondii ◽

Drug Target ◽

Drug Targets ◽

Protozoan Parasite ◽

World Population ◽

Content Type ◽

Tubulin Acetylation ◽

Parasite Replication ◽

New Treatments

ABSTRACT Toxoplasma gondii is an opportunistic parasite that infects at least one-third of the world population. New treatments for the disease (toxoplasmosis) are needed since current drugs are toxic to patients. Microtubules are essential cellular structures built from tubulin that show promise as antimicrobial drug targets. Microtubules can be regulated by chemical modification, such as acetylation on lysine 40 (K40). To determine the role of K40 acetylation in Toxoplasma and whether it is a liability to the parasite, we performed mutational analyses of the α-tubulin gene. Our results indicate that parasites cannot survive without K40 acetylation unless microtubules are stabilized with a secondary mutation. Additionally, we identified the parasite enzyme that acetylates α-tubulin (TgATAT). Genetic disruption of TgATAT caused severe defects in parasite replication, further highlighting the importance of α-tubulin K40 acetylation in Toxoplasma and its promise as a potential new drug target. Toxoplasma gondii is a widespread protozoan parasite that causes potentially life-threatening opportunistic disease. New inhibitors of parasite replication are urgently needed, as the current antifolate treatment is also toxic to patients. Microtubules are essential cytoskeletal components that have been selectively targeted in microbial pathogens; further study of tubulin in Toxoplasma may reveal novel therapeutic opportunities. It has been noted that α-tubulin acetylation at lysine 40 (K40) is enriched during daughter parasite formation, but the impact of this modification on Toxoplasma division and the enzyme mediating its delivery have not been identified. We performed mutational analyses to provide evidence that K40 acetylation stabilizes Toxoplasma microtubules and is required for parasite replication. We also show that an unusual Toxoplasma homologue of α-tubulin acetyltransferase (TgATAT) is expressed in a cell cycle-regulated manner and that its expression peaks during division. Disruption of TgATAT with CRISPR/Cas9 ablates K40 acetylation and induces replication defects; parasites appear to initiate mitosis yet exhibit incomplete or improper nuclear division. Together, these findings establish the importance of tubulin acetylation, exposing a new vulnerability in Toxoplasma that could be pharmacologically targeted. IMPORTANCE Toxoplasma gondii is an opportunistic parasite that infects at least one-third of the world population. New treatments for the disease (toxoplasmosis) are needed since current drugs are toxic to patients. Microtubules are essential cellular structures built from tubulin that show promise as antimicrobial drug targets. Microtubules can be regulated by chemical modification, such as acetylation on lysine 40 (K40). To determine the role of K40 acetylation in Toxoplasma and whether it is a liability to the parasite, we performed mutational analyses of the α-tubulin gene. Our results indicate that parasites cannot survive without K40 acetylation unless microtubules are stabilized with a secondary mutation. Additionally, we identified the parasite enzyme that acetylates α-tubulin (TgATAT). Genetic disruption of TgATAT caused severe defects in parasite replication, further highlighting the importance of α-tubulin K40 acetylation in Toxoplasma and its promise as a potential new drug target.

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