Unravelling the Sexual Developmental Biology of , a Model for Comparative Coccidian Parasite Studies

Overview

Journal Front Cell Infect Microbiol

Specialties Cell Biology
Infectious Diseases
Microbiology

Date 2023 Nov 13

PMID 37953800

Authors

Teresa Cruz-Bustos

Marlies Dolezal

Anna Sophia Feix

Barbel Ruttkowski

Karin Hummel

Ebrahim Razzazi-Fazeli

Anja Joachim

Affiliations

Soon will be listed here.

Abstract

Introduction: The apicomplexan parasite has global significance as an enteropathogen of suckling piglets. Its intricate life cycle entails a transition from an asexual phase to sexual development, ultimately leading to the formation of transmissible oocysts.

Methods: To advance our understanding of the parasite's cellular development, we complemented previous transcriptome studies by delving into the proteome profiles at five distinct time points of cultivation through LC/MS-MS analysis.

Results: A total of 1,324 proteins were identified in the developmental stages of , and 1,082 proteins were identified as significantly differentially expressed. Data are available via ProteomeXchange with identifier PXD045050. We performed BLAST, GO enrichment, and KEGG pathway analyses on the up- and downregulated proteins to elucidate correlated events in the life cycle. Our analyses revealed intriguing metabolic patterns in macromolecule metabolism, DNA- and RNA-related processes, proteins associated with sexual stages, and those involved in cell invasion, reflecting the adaptation of sexual stages to a nutrient-poor and potentially stressful extracellular environment, with a focus on enzymes involved in metabolism and energy production.

Discussion: These findings have important implications for understanding the developmental biology of as well as other, related coccidian parasites, such as spp. and . They also support the role of as a new model for the comparative biology of coccidian tissue cyst stages.

Citing Articles

An in-depth exploration of the multifaceted roles of EVs in the context of pathogenic single-cell microorganisms.

Feix A, Tabaie E, Singh A, Wittenberg N, Wilson E, Joachim A Microbiol Mol Biol Rev. 2024; 88(3):e0003724.

PMID: 38869292 PMC: 11426017. DOI: 10.1128/mmbr.00037-24.

The Evolution of Transglutaminases Underlies the Origin and Loss of Cornified Skin Appendages in Vertebrates.

Sachslehner A, Surbek M, Holthaus K, Steinbinder J, Golabi B, Hess C Mol Biol Evol. 2024; 41(6).

PMID: 38781495 PMC: 11152450. DOI: 10.1093/molbev/msae100.

References

Jacot D, Waller R, Soldati-Favre D, MacPherson D, MacRae J . Apicomplexan Energy Metabolism: Carbon Source Promiscuity and the Quiescence Hyperbole. Trends Parasitol. 2015; 32(1):56-70. DOI: 10.1016/j.pt.2015.09.001. View

Harding C, Frischknecht F . The Riveting Cellular Structures of Apicomplexan Parasites. Trends Parasitol. 2020; 36(12):979-991. DOI: 10.1016/j.pt.2020.09.001. View

Ferguson D, Sahoo N, Pinches R, Bumstead J, Tomley F, Gubbels M . MORN1 has a conserved role in asexual and sexual development across the apicomplexa. Eukaryot Cell. 2008; 7(4):698-711. PMC: 2292627. DOI: 10.1128/EC.00021-08. View

Walker R, Sharman P, Miller C, Lippuner C, Okoniewski M, Eichenberger R . RNA Seq analysis of the Eimeria tenella gametocyte transcriptome reveals clues about the molecular basis for sexual reproduction and oocyst biogenesis. BMC Genomics. 2015; 16:94. PMC: 4345034. DOI: 10.1186/s12864-015-1298-6. View

Zhang X, Smits A, van Tilburg G, Ovaa H, Huber W, Vermeulen M . Proteome-wide identification of ubiquitin interactions using UbIA-MS. Nat Protoc. 2018; 13(3):530-550. DOI: 10.1038/nprot.2017.147. View

Ferguson D, HUTCHISON W, SIIM J . The ultrastructural development of the macrogamete and formation of the oocyst wall of Toxoplasma gondii. Acta Pathol Microbiol Scand B. 1975; 83(5):491-505. DOI: 10.1111/j.1699-0463.1975.tb00130.x. View

de Monerri N, Yakubu R, Chen A, Bradley P, Nieves E, Weiss L . The Ubiquitin Proteome of Toxoplasma gondii Reveals Roles for Protein Ubiquitination in Cell-Cycle Transitions. Cell Host Microbe. 2015; 18(5):621-33. PMC: 4968887. DOI: 10.1016/j.chom.2015.10.014. View

Dalmasso M, Echeverria P, Zappia M, Hellman U, Dubremetz J, Angel S . Toxoplasma gondii has two lineages of histones 2b (H2B) with different expression profiles. Mol Biochem Parasitol. 2006; 148(1):103-7. DOI: 10.1016/j.molbiopara.2006.03.005. View

Chion M, Carapito C, Bertrand F . Towards a More Accurate Differential Analysis of Multiple Imputed Proteomics Data with mi4limma. Methods Mol Biol. 2022; 2426:131-140. DOI: 10.1007/978-1-0716-1967-4_7. View

10.

Dalmasso M, Onyango D, Naguleswaran A, Sullivan Jr W, Angel S . Toxoplasma H2A variants reveal novel insights into nucleosome composition and functions for this histone family. J Mol Biol. 2009; 392(1):33-47. PMC: 2734877. DOI: 10.1016/j.jmb.2009.07.017. View

11.

Painter H, Campbell T, Llinas M . The Apicomplexan AP2 family: integral factors regulating Plasmodium development. Mol Biochem Parasitol. 2010; 176(1):1-7. PMC: 3026892. DOI: 10.1016/j.molbiopara.2010.11.014. View

12.

Hehl A, Basso W, Lippuner C, Ramakrishnan C, Okoniewski M, Walker R . Asexual expansion of Toxoplasma gondii merozoites is distinct from tachyzoites and entails expression of non-overlapping gene families to attach, invade, and replicate within feline enterocytes. BMC Genomics. 2015; 16:66. PMC: 4340605. DOI: 10.1186/s12864-015-1225-x. View

13.

Kim K . The Epigenome, Cell Cycle, and Development in Toxoplasma. Annu Rev Microbiol. 2018; 72:479-499. DOI: 10.1146/annurev-micro-090817-062741. View

14.

Shunmugam S, Arnold C, Dass S, Katris N, Botte C . The flexibility of Apicomplexa parasites in lipid metabolism. PLoS Pathog. 2022; 18(3):e1010313. PMC: 8929637. DOI: 10.1371/journal.ppat.1010313. View

15.

Fritz H, Bowyer P, Bogyo M, Conrad P, Boothroyd J . Proteomic analysis of fractionated Toxoplasma oocysts reveals clues to their environmental resistance. PLoS One. 2012; 7(1):e29955. PMC: 3261165. DOI: 10.1371/journal.pone.0029955. View

16.

Kloehn J, Hammoudi P, Soldati-Favre D . Metabolite salvage and restriction during infection - a tug of war between Toxoplasma gondii and its host. Curr Opin Biotechnol. 2020; 68:104-114. DOI: 10.1016/j.copbio.2020.09.015. View

17.

Martorelli di Genova B, Knoll L . Comparisons of the Sexual Cycles for the Coccidian Parasites and . Front Cell Infect Microbiol. 2020; 10:604897. PMC: 7768002. DOI: 10.3389/fcimb.2020.604897. View

18.

Zhang M, Joyce B, Sullivan Jr W, Nussenzweig V . Translational control in Plasmodium and toxoplasma parasites. Eukaryot Cell. 2012; 12(2):161-7. PMC: 3571306. DOI: 10.1128/EC.00296-12. View

19.

Massimine K, Doan L, Atreya C, Stedman T, Anderson K, Joiner K . Toxoplasma gondii is capable of exogenous folate transport. A likely expansion of the BT1 family of transmembrane proteins. Mol Biochem Parasitol. 2005; 144(1):44-54. DOI: 10.1016/j.molbiopara.2005.07.006. View

20.

Possenti A, Cherchi S, Bertuccini L, Pozio E, Dubey J, Spano F . Molecular characterisation of a novel family of cysteine-rich proteins of Toxoplasma gondii and ultrastructural evidence of oocyst wall localisation. Int J Parasitol. 2010; 40(14):1639-49. DOI: 10.1016/j.ijpara.2010.06.009. View