Skip to main content
Log in

Evolution of Plant-Like Crystalline Storage Polysaccharide in the Protozoan Parasite Toxoplasma gondii Argues for a Red Alga Ancestry

  • Published:
Journal of Molecular Evolution Aims and scope Submit manuscript

Abstract

Single-celled apicomplexan parasites are known to cause major diseases in humans and animals including malaria, toxoplasmosis, and coccidiosis. The presence of apicoplasts with the remnant of a plastid-like DNA argues that these parasites evolved from photosynthetic ancestors possibly related to the dinoflagellates. Toxoplasma gondii displays amylopectin-like polymers within the cytoplasm of the dormant brain cysts. Here we report a detailed structural and comparative analysis of the Toxoplasma gondii, green alga Chlamydomonas reinhardtii, and dinoflagellate Crypthecodinium cohnii storage polysaccharides. We show Toxoplasma gondii amylopectin to be similar to the semicrystalline floridean starch accumulated by red algae. Unlike green plants or algae, the nuclear DNA sequences as well as biochemical and phylogenetic analysis argue that the Toxoplasma gondii amylopectin pathway has evolved from a totally different UDP-glucose-based metabolism similar to that of the floridean starch accumulating red alga Cyanidioschyzon merolae and, to a lesser extent, to those of glycogen storing animals or fungi. In both red algae and apicomplexan parasites, isoamylase and glucan–water dikinase sequences are proposed to explain the appearance of semicrystalline starch-like polymers. Our results have built a case for the separate evolution of semicrystalline storage polysaccharides upon acquisition of photosynthesis in eukaryotes.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Figure 1
Figure 2
Figure 3
Figure 4
Figure 5
Figure 6
Figure 7
Figure 8
Figure 9

Similar content being viewed by others

References

  • SG Ball MK Morell (2003) ArticleTitleFrom bacterial glycogen to starch: understanding the biogenesis of the plant starch granule Annu Rev Plant Biol 54 207–233

    Google Scholar 

  • AA Ballicora MA Iglesias J Preiss (2003) ArticleTitleADP-glucose pyrophosphorylase, a regulatory enzyme for bacterial glycogen synthesis Microbiol Mol Biol Rev 67 213–225

    Google Scholar 

  • A Buléon D-J Gallant B Bouchet G Mouille C D’Hulst J Kossman SG Ball (1997) ArticleTitleStarches from A to C. Chlamydomonas reinhardtii as a model microbial system to investigate the biosynthesis of the plant amylopectin crystal Plant Physiol 115 949–957

    Google Scholar 

  • X Cai AL Fuller LR McDougald G Zhu (2003) ArticleTitleApicoplast genome of the coccidian Eimeria tenella Gene 321 39–46

    Google Scholar 

  • T Cavalier-Smith (1999) ArticleTitlePrinciples of protein targeting in secondary symbiogenesis: euglenoid, dinoflagellate and sporozoan plastid origins and the eukaryote family tree J Euk Microbiol 46 347–366

    Google Scholar 

  • C Colleoni D Dauvillee G Mouille A Buleon D Gallant B Bouchet M Morell M Samuel B Delrue C d’Hulst C Bliard JM Nuzillard S Ball (1999) ArticleTitleGenetic and biochemical evidence for the involvement of alpha-1, 4-glucanotransferases in amylopectin synthesis Plant Physiol 120 993–1004

    Google Scholar 

  • SE Douglas SL Penny (1999) ArticleTitleThe plastid genome of the cryptophyte alga, Guillardia theta: complete sequence and conserved synteny groups confirm its common ancestry with red algae J Mol Evol 48 236–244 Occurrence Handle1:CAS:528:DyaK1MXotVyqsQ%3D%3D Occurrence Handle9929392

    CAS  PubMed  Google Scholar 

  • F Dzierszinski O Popescu C Toursel C Slomianny B Yahiaoui S Tomavo (1999) ArticleTitleThe protozoan parasite Toxoplasma gondii expresses two functional plant-like glycolytic enzymes. Implications for evolutionary origin of apicomplexans J Biol Chem 274 24888–24895

    Google Scholar 

  • F Dzierszinski M Mortuaire N Dendouga O Popescu S Tomavo (2001) ArticleTitleDifferential expression of two plant-like enolases with distinct enzymatic and antigenic properties during stage conversion of the protozoan parasite Toxoplasma gondii J Mol Biol 309 1017–1027 Occurrence Handle10.1006/jmbi.2001.4730 Occurrence Handle1:CAS:528:DC%2BD3MXkt1Sgsbc%3D Occurrence Handle11399076

    Article  CAS  PubMed  Google Scholar 

  • NM Fast JC Kissinger DS Roos PJ Keeling (2001) ArticleTitleNuclear-encoded, plastid-targeted genes suggest a single common origin for apicomplexan and dinoflagellate plastids Mol Biol Evol 18 418–426 Occurrence Handle1:CAS:528:DC%2BD3MXhvVKrt78%3D Occurrence Handle11230543

    CAS  PubMed  Google Scholar 

  • S Funes E Davidson A Reyes-Prieto S Magallon P Herion MP King D Gonzalez-Halphen (2002) ArticleTitleA green algal apicoplast ancestor Science 298 2155

    Google Scholar 

  • E Greenberg J Preiss (1964) ArticleTitleThe occurrence of adenosine diphosphate glucose: glycogen transglucosylase in bacteria J Biol Chem 239 4314–4315

    Google Scholar 

  • JR Harris M Adrian F Petry (2004) ArticleTitleAmylopectin: a major component of the residual body in Cryptosporidium parvum oocysts Parasitology 128 269–282

    Google Scholar 

  • B Henrissat E Deleury PM Coutinho (2002) ArticleTitleGlycogen metabolism loss: a common marker of parasitic behaviour in bacteria? Trends Genet 18 437–440

    Google Scholar 

  • YD Karkhanis JJ Allocco DM Schmatz (1993) ArticleTitleAmylopectin synthase of Eimeria tenella: identification and kinetic characterization J Euk Microbiol 40 594–598

    Google Scholar 

  • S Köhler CF Delwiche PW Denny LG Tilney P Webster RJ Wilson JD Palmer DS Roos (1997) ArticleTitleA plastid of probable green algal origin in apicomplexan parasites Science 275 1485–1489

    Google Scholar 

  • N Libessart ML Maddelein N Koornhuyse ParticleVan den A Decq B Delrue G Mouille C D’Hulst S Ball (1995) ArticleTitleStorage, photosynthesis, and growth: the conditional nature of mutations affecting starch synthesis and structure in Chlamydomonas Plant Cell 7 1117–1127

    Google Scholar 

  • BJ Luft JS Remington (1988) ArticleTitleAIDS commentary. Toxoplasmic encephalitis J Infect Dis 157 1–6

    Google Scholar 

  • BJ Luft JS Remington (1992) ArticleTitleToxoplasmic encephalitis in AIDS Clin Infect Dis 15 211–222 Occurrence Handle1:STN:280:By2A1M3psVE%3D Occurrence Handle1520757

    CAS  PubMed  Google Scholar 

  • E Marechal MF Cesbron-Delauw (2001) ArticleTitleThe apicoplast: a new member of the plastid family Trends Plant Sci 6 200–205

    Google Scholar 

  • M Matsuzaki O Misumi IT Shin S Maruyama et al. (2004) ArticleTitleGenome sequence of the ultrasmall unicellular red alga Cyanidioschyzon merolae 10D Nature 428 653–657

    Google Scholar 

  • GI McFadden ME Reith J Munholland N Lang-Unnasch (1996) ArticleTitlePlastid in human parasites Nature 381 482

    Google Scholar 

  • P Nyvall J Pelloux HV Davies M Pedersen R Viola (1999) ArticleTitlePurification and characterisation of a novel starch synthase selective for uridine 5′-diphosphate glucose from the red alga Gracilaria tenuistipitata Planta 209 143–152

    Google Scholar 

  • E Perret J Davoust M Albert L Besseau M-O Soyer-Gobillard (1993) ArticleTitleMicrotubule organization during the cell cycle of the primitive eukaryote dinoflagellate Crypthecodinium cohnii J Cell Sci 104 639–651

    Google Scholar 

  • JP Ral E Derelle C Ferraz F Wattebled B Farinas F Corellou A Buléon MC Slomianny D Delvalle C d’Hulst S Rombauts H Moreau S Ball (2004) ArticleTitleStarch division and partitioning a mechanism for granule propagation and maintenance in the picophytoplanktonic green alga Ostreococcus tauri Plant Physiol 36 3333–3340

    Google Scholar 

  • E Recondo L Leloir (1961) ArticleTitleAdenosine diphosphate glucose and starch biosynthesis Biochem Biophys Res Commun 6 85–88

    Google Scholar 

  • G Ritte JR Lloyd N Eckermann A Rottmann J Kossmann M Steup (2002) ArticleTitleThe starch-related R1 protein is an alpha-glucan, water dikinase Proc Natl Acad Sci USA 99 7166–7171

    Google Scholar 

  • JF Ryley M Bentley DJ Manners JR Stark (1969) ArticleTitleAmylopectin, the storage polysaccharide of the coccidian Eimeria brunetti and E. tenella J Parasitol 55 839–845

    Google Scholar 

  • F Seeber (1997) ArticleTitleConsensus sequence of translational initiation sites from Toxoplasma gondii genes Parasitol Res 83 309–311

    Google Scholar 

  • JD Thompson DG Higgins TJ Gibson (1994) ArticleTitleClustalW: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice Nucleic Acids Res 22 4673–4680 Occurrence Handle1:CAS:528:DyaK2MXitlSgu74%3D Occurrence Handle7984417

    CAS  PubMed  Google Scholar 

  • S Tomavo (2001) ArticleTitleThe differential expression of multiple isoenzyme forms during stage conversion of Toxoplasma gondii: an adaptive developmental strategy Int J Parasitol 31 1023–1031 Occurrence Handle10.1016/S0020-7519(01)00193-X Occurrence Handle1:CAS:528:DC%2BD3MXks1OjtLw%3D Occurrence Handle11429165

    Article  CAS  PubMed  Google Scholar 

  • R Viola P Nyvall M Pedersen (2001) ArticleTitleThe unique features of starch metabolism in red algae Proc R Soc Lond B Biol Sci 268 1417–1422

    Google Scholar 

  • RF Waller PJ Keeling GG Dooren ParticleVan GI McFadden (2003) ArticleTitleComment on a green algal apicoplast ancestor Science 301 49

    Google Scholar 

  • RJM Wilson PW Denny PR Preiser K Rangachari K Roberts A Roy A Whyte M Strath DJ Moore PW Moore DH Williamson (1996) ArticleTitleComplete gene map of the plastid-like DNA of the malaria parasite Plasmodium falciparum J Mol Biol 261 155–172 Occurrence Handle10.1006/jmbi.1996.0449 Occurrence Handle1:CAS:528:DyaK28XltFKrsbw%3D Occurrence Handle8757284

    Article  CAS  PubMed  Google Scholar 

  • Z Zhang BR Green T Cavalier-Smith (1999) ArticleTitleSingle gene circles in dinoflagellate chloroplast genomes Nature 400 155–159

    Google Scholar 

Download references

Acknowledgments

For comments, logistical support, and invaluable technical assistance in the field and lab, we thank Michael Kibe, Marléne Mortuaire, Hervé Moreau, Christian Slomianny, Emmanuel Maes, Frédéric Chirat, Yves Leroy, Florence Dzierszinski, Brigitte Bouchet, and Bruno Pontoire. We acknowledge the Toxoplasma Genome Sequencing Consortium for making available the genome database: Preliminary genomic and/or cDNA sequence data were accessed via http://ToxoDB.org and/or http://www.tigr.org/tdb/t_gondii/. Genomic data were provided by The Institute for Genomic Research (supported by NIH Grant AI05093), and by the Sanger Center (Wellcome Trust). EST sequences were generated by Washington University (NIH Grant 1R01AI045806-01A1). This research was funded by the Centre National de la Recherche Scientifique (CNRS) through the Action Thématique Incitative sur Programme et Equipe (ATIPE), the Programme Inter-organisme de Microbiologie Fondamentale, and the Agence Nationale de la Recherche sur le Sida (ANRS).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Stanislas Tomavo.

Additional information

Reviewing Editor:Dr. Patrick Keeling

Appendix: Supplementary material

Rights and permissions

Reprints and permissions

About this article

Cite this article

Coppin, A., Varré, JS., Lienard, L. et al. Evolution of Plant-Like Crystalline Storage Polysaccharide in the Protozoan Parasite Toxoplasma gondii Argues for a Red Alga Ancestry. J Mol Evol 60, 257–267 (2005). https://doi.org/10.1007/s00239-004-0185-6

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00239-004-0185-6

Keywords

Navigation