Multiple Independent Origins of Apicomplexan-Like Parasites

Varsha Mathur; Martin Kolísko; Elisabeth Hehenberger; Nicholas A.T. Irwin; Brian S. Leander; Árni Kristmundsson; Mark A. Freeman; Patrick J. Keeling

doi:10.1016/j.cub.2019.07.019

Multiple Independent Origins of Apicomplexan-Like Parasites

Varsha Mathur^*, Martin Kolísko, Elisabeth Hehenberger, Nicholas A.T. Irwin, Brian S. Leander, Árni Kristmundsson, Mark A. Freeman, Patrick J. Keeling

^*Corresponding author for this work

University of Iceland

Research output: Contribution to journal › Article › peer-review

21 Citations (Scopus)

Abstract

The apicomplexans are a group of obligate animal pathogens that include Plasmodium (malaria), Toxoplasma (toxoplasmosis), and Cryptosporidium (cryptosporidiosis) [1]. They are an extremely diverse and specious group but are nevertheless united by a distinctive suite of cytoskeletal and secretory structures related to infection, called the apical complex, which is used to recognize and gain entry into animal host cells. The apicomplexans are also known to have evolved from free-living photosynthetic ancestors and retain a relict plastid (the apicoplast), which is non-photosynthetic but houses a number of other essential metabolic pathways [2]. Their closest relatives include a mix of both photosynthetic algae (chromerids) and non-photosynthetic microbial predators (colpodellids) [3]. Genomic analyses of these free-living relatives have revealed a great deal about how the alga-parasite transition may have taken place, as well as origins of parasitism more generally [4]. Here, we show that, despite the surprisingly complex origin of apicomplexans from algae, this transition actually occurred at least three times independently. Using single-cell genomics and transcriptomics from diverse uncultivated parasites, we find that two genera previously classified within the Apicomplexa, Piridium and Platyproteum, form separately branching lineages in phylogenomic analyses. Both retain cryptic plastids with genomic and metabolic features convergent with apicomplexans. These findings suggest a predilection in this lineage for both the convergent loss of photosynthesis and transition to parasitism, resulting in multiple lineages of superficially similar animal parasites.

Original language	English
Pages (from-to)	2936-2941.e5
Journal	Current Biology
Volume	29
Issue number	17
DOIs	https://doi.org/10.1016/j.cub.2019.07.019
Publication status	Published - 9 Sept 2019

Bibliographical note

Funding Information:
We thank Maria Herranz, Niels van Steenkiste, Phil Angel, and the Hakai Institute for their assistance in sample collection. We also thank Filip Husnik for his guidance with the transcriptomics and Waldan Kwong for his valuable feedback on the manuscript. This work was supported by grants from the Canadian Institutes for Health Research ( MOP-42517 ) to P.J.K. and HIR grant ( UMC/625/1/HIR/027 ) to M.A.F. from the University of Malaya, Kuala Lumpur . M.K. was supported by a grant to the Centre for Microbial Diversity and Evolution from the Tula Foundation , the ERD fund “Centre for Research of Pathogenicity and Virulence of Parasites” (no. CZ.02.1.01/0.0/0.0/16_019/0000759 ), and Fellowship Purkyne, Czech Acad. Sci. N.A.T.I. was supported by an NSERC Canadian Graduate Scholarship.

Funding Information:
We thank Maria Herranz, Niels van Steenkiste, Phil Angel, and the Hakai Institute for their assistance in sample collection. We also thank Filip Husnik for his guidance with the transcriptomics and Waldan Kwong for his valuable feedback on the manuscript. This work was supported by grants from the Canadian Institutes for Health Research (MOP-42517) to P.J.K. and HIR grant (UMC/625/1/HIR/027) to M.A.F. from the University of Malaya, Kuala Lumpur. M.K. was supported by a grant to the Centre for Microbial Diversity and Evolution from the Tula Foundation, the ERD fund ?Centre for Research of Pathogenicity and Virulence of Parasites? (no. CZ.02.1.01/0.0/0.0/16_019/0000759), and Fellowship Purkyne, Czech Acad. Sci. N.A.T.I. was supported by an NSERC Canadian Graduate Scholarship. V.M. M.K. and P.J.K. designed the study. V.M. ?.K. M.A.F. and B.S.L. obtained samples. M.A.F. and ?.K. performed the initial molecular diagnosis for Piridium. V.M. M.K. and N.A.T.I. conducted genomics, transcriptomics, and phylogenomics. E.H. N.A.T.I. M.K. and V.M. performed plastid analyses. V.M. and M.K. performed all other analyses. V.M. M.K. and P.J.K. wrote the manuscript with input from all authors. The authors declare no competing interests.

Publisher Copyright:
© 2019 Elsevier Ltd

Other keywords

apicomplexans
convergent evolution
genome
gregarines
parasitism
phylogenomics
plastid
transcriptome

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10.1016/j.cub.2019.07.019

Cite this

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title = "Multiple Independent Origins of Apicomplexan-Like Parasites",

abstract = "The apicomplexans are a group of obligate animal pathogens that include Plasmodium (malaria), Toxoplasma (toxoplasmosis), and Cryptosporidium (cryptosporidiosis) [1]. They are an extremely diverse and specious group but are nevertheless united by a distinctive suite of cytoskeletal and secretory structures related to infection, called the apical complex, which is used to recognize and gain entry into animal host cells. The apicomplexans are also known to have evolved from free-living photosynthetic ancestors and retain a relict plastid (the apicoplast), which is non-photosynthetic but houses a number of other essential metabolic pathways [2]. Their closest relatives include a mix of both photosynthetic algae (chromerids) and non-photosynthetic microbial predators (colpodellids) [3]. Genomic analyses of these free-living relatives have revealed a great deal about how the alga-parasite transition may have taken place, as well as origins of parasitism more generally [4]. Here, we show that, despite the surprisingly complex origin of apicomplexans from algae, this transition actually occurred at least three times independently. Using single-cell genomics and transcriptomics from diverse uncultivated parasites, we find that two genera previously classified within the Apicomplexa, Piridium and Platyproteum, form separately branching lineages in phylogenomic analyses. Both retain cryptic plastids with genomic and metabolic features convergent with apicomplexans. These findings suggest a predilection in this lineage for both the convergent loss of photosynthesis and transition to parasitism, resulting in multiple lineages of superficially similar animal parasites.",

keywords = "apicomplexans, convergent evolution, genome, gregarines, parasitism, phylogenomics, plastid, transcriptome",

author = "Varsha Mathur and Martin Kol{\'i}sko and Elisabeth Hehenberger and Irwin, {Nicholas A.T.} and Leander, {Brian S.} and {\'A}rni Kristmundsson and Freeman, {Mark A.} and Keeling, {Patrick J.}",

note = "Funding Information: We thank Maria Herranz, Niels van Steenkiste, Phil Angel, and the Hakai Institute for their assistance in sample collection. We also thank Filip Husnik for his guidance with the transcriptomics and Waldan Kwong for his valuable feedback on the manuscript. This work was supported by grants from the Canadian Institutes for Health Research ( MOP-42517 ) to P.J.K. and HIR grant ( UMC/625/1/HIR/027 ) to M.A.F. from the University of Malaya, Kuala Lumpur . M.K. was supported by a grant to the Centre for Microbial Diversity and Evolution from the Tula Foundation , the ERD fund “Centre for Research of Pathogenicity and Virulence of Parasites” (no. CZ.02.1.01/0.0/0.0/16_019/0000759 ), and Fellowship Purkyne, Czech Acad. Sci. N.A.T.I. was supported by an NSERC Canadian Graduate Scholarship. Funding Information: We thank Maria Herranz, Niels van Steenkiste, Phil Angel, and the Hakai Institute for their assistance in sample collection. We also thank Filip Husnik for his guidance with the transcriptomics and Waldan Kwong for his valuable feedback on the manuscript. This work was supported by grants from the Canadian Institutes for Health Research (MOP-42517) to P.J.K. and HIR grant (UMC/625/1/HIR/027) to M.A.F. from the University of Malaya, Kuala Lumpur. M.K. was supported by a grant to the Centre for Microbial Diversity and Evolution from the Tula Foundation, the ERD fund ?Centre for Research of Pathogenicity and Virulence of Parasites? (no. CZ.02.1.01/0.0/0.0/16_019/0000759), and Fellowship Purkyne, Czech Acad. Sci. N.A.T.I. was supported by an NSERC Canadian Graduate Scholarship. V.M. M.K. and P.J.K. designed the study. V.M. ?.K. M.A.F. and B.S.L. obtained samples. M.A.F. and ?.K. performed the initial molecular diagnosis for Piridium. V.M. M.K. and N.A.T.I. conducted genomics, transcriptomics, and phylogenomics. E.H. N.A.T.I. M.K. and V.M. performed plastid analyses. V.M. and M.K. performed all other analyses. V.M. M.K. and P.J.K. wrote the manuscript with input from all authors. The authors declare no competing interests. Publisher Copyright: {\textcopyright} 2019 Elsevier Ltd",

year = "2019",

month = sep,

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doi = "10.1016/j.cub.2019.07.019",

language = "English",

volume = "29",

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AU - Kolísko, Martin

AU - Hehenberger, Elisabeth

AU - Irwin, Nicholas A.T.

AU - Leander, Brian S.

AU - Kristmundsson, Árni

AU - Freeman, Mark A.

AU - Keeling, Patrick J.

N1 - Funding Information: We thank Maria Herranz, Niels van Steenkiste, Phil Angel, and the Hakai Institute for their assistance in sample collection. We also thank Filip Husnik for his guidance with the transcriptomics and Waldan Kwong for his valuable feedback on the manuscript. This work was supported by grants from the Canadian Institutes for Health Research ( MOP-42517 ) to P.J.K. and HIR grant ( UMC/625/1/HIR/027 ) to M.A.F. from the University of Malaya, Kuala Lumpur . M.K. was supported by a grant to the Centre for Microbial Diversity and Evolution from the Tula Foundation , the ERD fund “Centre for Research of Pathogenicity and Virulence of Parasites” (no. CZ.02.1.01/0.0/0.0/16_019/0000759 ), and Fellowship Purkyne, Czech Acad. Sci. N.A.T.I. was supported by an NSERC Canadian Graduate Scholarship. Funding Information: We thank Maria Herranz, Niels van Steenkiste, Phil Angel, and the Hakai Institute for their assistance in sample collection. We also thank Filip Husnik for his guidance with the transcriptomics and Waldan Kwong for his valuable feedback on the manuscript. This work was supported by grants from the Canadian Institutes for Health Research (MOP-42517) to P.J.K. and HIR grant (UMC/625/1/HIR/027) to M.A.F. from the University of Malaya, Kuala Lumpur. M.K. was supported by a grant to the Centre for Microbial Diversity and Evolution from the Tula Foundation, the ERD fund ?Centre for Research of Pathogenicity and Virulence of Parasites? (no. CZ.02.1.01/0.0/0.0/16_019/0000759), and Fellowship Purkyne, Czech Acad. Sci. N.A.T.I. was supported by an NSERC Canadian Graduate Scholarship. V.M. M.K. and P.J.K. designed the study. V.M. ?.K. M.A.F. and B.S.L. obtained samples. M.A.F. and ?.K. performed the initial molecular diagnosis for Piridium. V.M. M.K. and N.A.T.I. conducted genomics, transcriptomics, and phylogenomics. E.H. N.A.T.I. M.K. and V.M. performed plastid analyses. V.M. and M.K. performed all other analyses. V.M. M.K. and P.J.K. wrote the manuscript with input from all authors. The authors declare no competing interests. Publisher Copyright: © 2019 Elsevier Ltd

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N2 - The apicomplexans are a group of obligate animal pathogens that include Plasmodium (malaria), Toxoplasma (toxoplasmosis), and Cryptosporidium (cryptosporidiosis) [1]. They are an extremely diverse and specious group but are nevertheless united by a distinctive suite of cytoskeletal and secretory structures related to infection, called the apical complex, which is used to recognize and gain entry into animal host cells. The apicomplexans are also known to have evolved from free-living photosynthetic ancestors and retain a relict plastid (the apicoplast), which is non-photosynthetic but houses a number of other essential metabolic pathways [2]. Their closest relatives include a mix of both photosynthetic algae (chromerids) and non-photosynthetic microbial predators (colpodellids) [3]. Genomic analyses of these free-living relatives have revealed a great deal about how the alga-parasite transition may have taken place, as well as origins of parasitism more generally [4]. Here, we show that, despite the surprisingly complex origin of apicomplexans from algae, this transition actually occurred at least three times independently. Using single-cell genomics and transcriptomics from diverse uncultivated parasites, we find that two genera previously classified within the Apicomplexa, Piridium and Platyproteum, form separately branching lineages in phylogenomic analyses. Both retain cryptic plastids with genomic and metabolic features convergent with apicomplexans. These findings suggest a predilection in this lineage for both the convergent loss of photosynthesis and transition to parasitism, resulting in multiple lineages of superficially similar animal parasites.

AB - The apicomplexans are a group of obligate animal pathogens that include Plasmodium (malaria), Toxoplasma (toxoplasmosis), and Cryptosporidium (cryptosporidiosis) [1]. They are an extremely diverse and specious group but are nevertheless united by a distinctive suite of cytoskeletal and secretory structures related to infection, called the apical complex, which is used to recognize and gain entry into animal host cells. The apicomplexans are also known to have evolved from free-living photosynthetic ancestors and retain a relict plastid (the apicoplast), which is non-photosynthetic but houses a number of other essential metabolic pathways [2]. Their closest relatives include a mix of both photosynthetic algae (chromerids) and non-photosynthetic microbial predators (colpodellids) [3]. Genomic analyses of these free-living relatives have revealed a great deal about how the alga-parasite transition may have taken place, as well as origins of parasitism more generally [4]. Here, we show that, despite the surprisingly complex origin of apicomplexans from algae, this transition actually occurred at least three times independently. Using single-cell genomics and transcriptomics from diverse uncultivated parasites, we find that two genera previously classified within the Apicomplexa, Piridium and Platyproteum, form separately branching lineages in phylogenomic analyses. Both retain cryptic plastids with genomic and metabolic features convergent with apicomplexans. These findings suggest a predilection in this lineage for both the convergent loss of photosynthesis and transition to parasitism, resulting in multiple lineages of superficially similar animal parasites.

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KW - gregarines

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KW - plastid

KW - transcriptome

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ER -

Multiple Independent Origins of Apicomplexan-Like Parasites

Abstract

Bibliographical note

Other keywords

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