Systems-Based Analysis of the <italic toggle="yes">Sarcocystis neurona</italic> Genome Identifies Pathways That Contribute to a Heteroxenous Life Cycle

ABSTRACT Sarcocystis neurona is a member of the coccidia, a clade of single-celled parasites of medical and veterinary importance including Eimeria, Sarcocystis, Neospora, and Toxoplasma. Unlike Eimeria, a single-host enteric pathogen, Sarcocystis, Neospora, and Toxoplasma are two-host parasites tha...

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Autores principales: Tomasz Blazejewski, Nirvana Nursimulu, Viviana Pszenny, Sriveny Dangoudoubiyam, Sivaranjani Namasivayam, Melissa A. Chiasson, Kyle Chessman, Michelle Tonkin, Lakshmipuram S. Swapna, Stacy S. Hung, Joshua Bridgers, Stacy M. Ricklefs, Martin J. Boulanger, Jitender P. Dubey, Stephen F. Porcella, Jessica C. Kissinger, Daniel K. Howe, Michael E. Grigg, John Parkinson
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Publicado: American Society for Microbiology 2015
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spelling oai:doaj.org-article:1b21fff66b5144da8b40c3091910cd882021-11-15T15:41:19ZSystems-Based Analysis of the <italic toggle="yes">Sarcocystis neurona</italic> Genome Identifies Pathways That Contribute to a Heteroxenous Life Cycle10.1128/mBio.02445-142150-7511https://doaj.org/article/1b21fff66b5144da8b40c3091910cd882015-02-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.02445-14https://doaj.org/toc/2150-7511ABSTRACT Sarcocystis neurona is a member of the coccidia, a clade of single-celled parasites of medical and veterinary importance including Eimeria, Sarcocystis, Neospora, and Toxoplasma. Unlike Eimeria, a single-host enteric pathogen, Sarcocystis, Neospora, and Toxoplasma are two-host parasites that infect and produce infectious tissue cysts in a wide range of intermediate hosts. As a genus, Sarcocystis is one of the most successful protozoan parasites; all vertebrates, including birds, reptiles, fish, and mammals are hosts to at least one Sarcocystis species. Here we sequenced Sarcocystis neurona, the causal agent of fatal equine protozoal myeloencephalitis. The S. neurona genome is 127 Mbp, more than twice the size of other sequenced coccidian genomes. Comparative analyses identified conservation of the invasion machinery among the coccidia. However, many dense-granule and rhoptry kinase genes, responsible for altering host effector pathways in Toxoplasma and Neospora, are absent from S. neurona. Further, S. neurona has a divergent repertoire of SRS proteins, previously implicated in tissue cyst formation in Toxoplasma. Systems-based analyses identified a series of metabolic innovations, including the ability to exploit alternative sources of energy. Finally, we present an S. neurona model detailing conserved molecular innovations that promote the transition from a purely enteric lifestyle (Eimeria) to a heteroxenous parasite capable of infecting a wide range of intermediate hosts. IMPORTANCE Sarcocystis neurona is a member of the coccidia, a clade of single-celled apicomplexan parasites responsible for major economic and health care burdens worldwide. A cousin of Plasmodium, Cryptosporidium, Theileria, and Eimeria, Sarcocystis is one of the most successful parasite genera; it is capable of infecting all vertebrates (fish, reptiles, birds, and mammals—including humans). The past decade has witnessed an increasing number of human outbreaks of clinical significance associated with acute sarcocystosis. Among Sarcocystis species, S. neurona has a wide host range and causes fatal encephalitis in horses, marine mammals, and several other mammals. To provide insights into the transition from a purely enteric parasite (e.g., Eimeria) to one that forms tissue cysts (Toxoplasma), we present the first genome sequence of S. neurona. Comparisons with other coccidian genomes highlight the molecular innovations that drive its distinct life cycle strategies.Tomasz BlazejewskiNirvana NursimuluViviana PszennySriveny DangoudoubiyamSivaranjani NamasivayamMelissa A. ChiassonKyle ChessmanMichelle TonkinLakshmipuram S. SwapnaStacy S. HungJoshua BridgersStacy M. RicklefsMartin J. BoulangerJitender P. DubeyStephen F. PorcellaJessica C. KissingerDaniel K. HoweMichael E. GriggJohn ParkinsonAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 6, Iss 1 (2015)
institution DOAJ
collection DOAJ
language EN
topic Microbiology
QR1-502
spellingShingle Microbiology
QR1-502
Tomasz Blazejewski
Nirvana Nursimulu
Viviana Pszenny
Sriveny Dangoudoubiyam
Sivaranjani Namasivayam
Melissa A. Chiasson
Kyle Chessman
Michelle Tonkin
Lakshmipuram S. Swapna
Stacy S. Hung
Joshua Bridgers
Stacy M. Ricklefs
Martin J. Boulanger
Jitender P. Dubey
Stephen F. Porcella
Jessica C. Kissinger
Daniel K. Howe
Michael E. Grigg
John Parkinson
Systems-Based Analysis of the <italic toggle="yes">Sarcocystis neurona</italic> Genome Identifies Pathways That Contribute to a Heteroxenous Life Cycle
description ABSTRACT Sarcocystis neurona is a member of the coccidia, a clade of single-celled parasites of medical and veterinary importance including Eimeria, Sarcocystis, Neospora, and Toxoplasma. Unlike Eimeria, a single-host enteric pathogen, Sarcocystis, Neospora, and Toxoplasma are two-host parasites that infect and produce infectious tissue cysts in a wide range of intermediate hosts. As a genus, Sarcocystis is one of the most successful protozoan parasites; all vertebrates, including birds, reptiles, fish, and mammals are hosts to at least one Sarcocystis species. Here we sequenced Sarcocystis neurona, the causal agent of fatal equine protozoal myeloencephalitis. The S. neurona genome is 127 Mbp, more than twice the size of other sequenced coccidian genomes. Comparative analyses identified conservation of the invasion machinery among the coccidia. However, many dense-granule and rhoptry kinase genes, responsible for altering host effector pathways in Toxoplasma and Neospora, are absent from S. neurona. Further, S. neurona has a divergent repertoire of SRS proteins, previously implicated in tissue cyst formation in Toxoplasma. Systems-based analyses identified a series of metabolic innovations, including the ability to exploit alternative sources of energy. Finally, we present an S. neurona model detailing conserved molecular innovations that promote the transition from a purely enteric lifestyle (Eimeria) to a heteroxenous parasite capable of infecting a wide range of intermediate hosts. IMPORTANCE Sarcocystis neurona is a member of the coccidia, a clade of single-celled apicomplexan parasites responsible for major economic and health care burdens worldwide. A cousin of Plasmodium, Cryptosporidium, Theileria, and Eimeria, Sarcocystis is one of the most successful parasite genera; it is capable of infecting all vertebrates (fish, reptiles, birds, and mammals—including humans). The past decade has witnessed an increasing number of human outbreaks of clinical significance associated with acute sarcocystosis. Among Sarcocystis species, S. neurona has a wide host range and causes fatal encephalitis in horses, marine mammals, and several other mammals. To provide insights into the transition from a purely enteric parasite (e.g., Eimeria) to one that forms tissue cysts (Toxoplasma), we present the first genome sequence of S. neurona. Comparisons with other coccidian genomes highlight the molecular innovations that drive its distinct life cycle strategies.
format article
author Tomasz Blazejewski
Nirvana Nursimulu
Viviana Pszenny
Sriveny Dangoudoubiyam
Sivaranjani Namasivayam
Melissa A. Chiasson
Kyle Chessman
Michelle Tonkin
Lakshmipuram S. Swapna
Stacy S. Hung
Joshua Bridgers
Stacy M. Ricklefs
Martin J. Boulanger
Jitender P. Dubey
Stephen F. Porcella
Jessica C. Kissinger
Daniel K. Howe
Michael E. Grigg
John Parkinson
author_facet Tomasz Blazejewski
Nirvana Nursimulu
Viviana Pszenny
Sriveny Dangoudoubiyam
Sivaranjani Namasivayam
Melissa A. Chiasson
Kyle Chessman
Michelle Tonkin
Lakshmipuram S. Swapna
Stacy S. Hung
Joshua Bridgers
Stacy M. Ricklefs
Martin J. Boulanger
Jitender P. Dubey
Stephen F. Porcella
Jessica C. Kissinger
Daniel K. Howe
Michael E. Grigg
John Parkinson
author_sort Tomasz Blazejewski
title Systems-Based Analysis of the <italic toggle="yes">Sarcocystis neurona</italic> Genome Identifies Pathways That Contribute to a Heteroxenous Life Cycle
title_short Systems-Based Analysis of the <italic toggle="yes">Sarcocystis neurona</italic> Genome Identifies Pathways That Contribute to a Heteroxenous Life Cycle
title_full Systems-Based Analysis of the <italic toggle="yes">Sarcocystis neurona</italic> Genome Identifies Pathways That Contribute to a Heteroxenous Life Cycle
title_fullStr Systems-Based Analysis of the <italic toggle="yes">Sarcocystis neurona</italic> Genome Identifies Pathways That Contribute to a Heteroxenous Life Cycle
title_full_unstemmed Systems-Based Analysis of the <italic toggle="yes">Sarcocystis neurona</italic> Genome Identifies Pathways That Contribute to a Heteroxenous Life Cycle
title_sort systems-based analysis of the <italic toggle="yes">sarcocystis neurona</italic> genome identifies pathways that contribute to a heteroxenous life cycle
publisher American Society for Microbiology
publishDate 2015
url https://doaj.org/article/1b21fff66b5144da8b40c3091910cd88
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