The genome of the obligate intracellular parasite Trachipleistophora hominis: new insights into microsporidian genome dynamics and reductive evolution.

The dynamics of reductive genome evolution for eukaryotes living inside other eukaryotic cells are poorly understood compared to well-studied model systems involving obligate intracellular bacteria. Here we present 8.5 Mb of sequence from the genome of the microsporidian Trachipleistophora hominis,...

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Autores principales:	Eva Heinz, Tom A Williams, Sirintra Nakjang, Christophe J Noël, Daniel C Swan, Alina V Goldberg, Simon R Harris, Thomas Weinmaier, Stephanie Markert, Dörte Becher, Jörg Bernhardt, Tal Dagan, Christian Hacker, John M Lucocq, Thomas Schweder, Thomas Rattei, Neil Hall, Robert P Hirt, T Martin Embley
Formato:	article
Lenguaje:	EN
Publicado:	Public Library of Science (PLoS) 2012
Materias:	Immunologic diseases. Allergy RC581-607 Biology (General) QH301-705.5
Acceso en línea:	https://doaj.org/article/998a2a319a7f43a396865ca1d01f48be
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spelling	oai:doaj.org-article:998a2a319a7f43a396865ca1d01f48be2021-11-18T06:06:26ZThe genome of the obligate intracellular parasite Trachipleistophora hominis: new insights into microsporidian genome dynamics and reductive evolution.1553-73661553-737410.1371/journal.ppat.1002979https://doaj.org/article/998a2a319a7f43a396865ca1d01f48be2012-01-01T00:00:00Zhttps://www.ncbi.nlm.nih.gov/pmc/articles/pmid/23133373/?tool=EBIhttps://doaj.org/toc/1553-7366https://doaj.org/toc/1553-7374The dynamics of reductive genome evolution for eukaryotes living inside other eukaryotic cells are poorly understood compared to well-studied model systems involving obligate intracellular bacteria. Here we present 8.5 Mb of sequence from the genome of the microsporidian Trachipleistophora hominis, isolated from an HIV/AIDS patient, which is an outgroup to the smaller compacted-genome species that primarily inform ideas of evolutionary mode for these enormously successful obligate intracellular parasites. Our data provide detailed information on the gene content, genome architecture and intergenic regions of a larger microsporidian genome, while comparative analyses allowed us to infer genomic features and metabolism of the common ancestor of the species investigated. Gene length reduction and massive loss of metabolic capacity in the common ancestor was accompanied by the evolution of novel microsporidian-specific protein families, whose conservation among microsporidians, against a background of reductive evolution, suggests they may have important functions in their parasitic lifestyle. The ancestor had already lost many metabolic pathways but retained glycolysis and the pentose phosphate pathway to provide cytosolic ATP and reduced coenzymes, and it had a minimal mitochondrion (mitosome) making Fe-S clusters but not ATP. It possessed bacterial-like nucleotide transport proteins as a key innovation for stealing host-generated ATP, the machinery for RNAi, key elements of the early secretory pathway, canonical eukaryotic as well as microsporidian-specific regulatory elements, a diversity of repetitive and transposable elements, and relatively low average gene density. Microsporidian genome evolution thus appears to have proceeded in at least two major steps: an ancestral remodelling of the proteome upon transition to intracellular parasitism that involved reduction but also selective expansion, followed by a secondary compaction of genome architecture in some, but not all, lineages.Eva HeinzTom A WilliamsSirintra NakjangChristophe J NoëlDaniel C SwanAlina V GoldbergSimon R HarrisThomas WeinmaierStephanie MarkertDörte BecherJörg BernhardtTal DaganChristian HackerJohn M LucocqThomas SchwederThomas RatteiNeil HallRobert P HirtT Martin EmbleyPublic Library of Science (PLoS)articleImmunologic diseases. AllergyRC581-607Biology (General)QH301-705.5ENPLoS Pathogens, Vol 8, Iss 10, p e1002979 (2012)
institution	DOAJ
collection	DOAJ
language	EN
topic	Immunologic diseases. Allergy RC581-607 Biology (General) QH301-705.5
spellingShingle	Immunologic diseases. Allergy RC581-607 Biology (General) QH301-705.5 Eva Heinz Tom A Williams Sirintra Nakjang Christophe J Noël Daniel C Swan Alina V Goldberg Simon R Harris Thomas Weinmaier Stephanie Markert Dörte Becher Jörg Bernhardt Tal Dagan Christian Hacker John M Lucocq Thomas Schweder Thomas Rattei Neil Hall Robert P Hirt T Martin Embley The genome of the obligate intracellular parasite Trachipleistophora hominis: new insights into microsporidian genome dynamics and reductive evolution.
description	The dynamics of reductive genome evolution for eukaryotes living inside other eukaryotic cells are poorly understood compared to well-studied model systems involving obligate intracellular bacteria. Here we present 8.5 Mb of sequence from the genome of the microsporidian Trachipleistophora hominis, isolated from an HIV/AIDS patient, which is an outgroup to the smaller compacted-genome species that primarily inform ideas of evolutionary mode for these enormously successful obligate intracellular parasites. Our data provide detailed information on the gene content, genome architecture and intergenic regions of a larger microsporidian genome, while comparative analyses allowed us to infer genomic features and metabolism of the common ancestor of the species investigated. Gene length reduction and massive loss of metabolic capacity in the common ancestor was accompanied by the evolution of novel microsporidian-specific protein families, whose conservation among microsporidians, against a background of reductive evolution, suggests they may have important functions in their parasitic lifestyle. The ancestor had already lost many metabolic pathways but retained glycolysis and the pentose phosphate pathway to provide cytosolic ATP and reduced coenzymes, and it had a minimal mitochondrion (mitosome) making Fe-S clusters but not ATP. It possessed bacterial-like nucleotide transport proteins as a key innovation for stealing host-generated ATP, the machinery for RNAi, key elements of the early secretory pathway, canonical eukaryotic as well as microsporidian-specific regulatory elements, a diversity of repetitive and transposable elements, and relatively low average gene density. Microsporidian genome evolution thus appears to have proceeded in at least two major steps: an ancestral remodelling of the proteome upon transition to intracellular parasitism that involved reduction but also selective expansion, followed by a secondary compaction of genome architecture in some, but not all, lineages.
format	article
author	Eva Heinz Tom A Williams Sirintra Nakjang Christophe J Noël Daniel C Swan Alina V Goldberg Simon R Harris Thomas Weinmaier Stephanie Markert Dörte Becher Jörg Bernhardt Tal Dagan Christian Hacker John M Lucocq Thomas Schweder Thomas Rattei Neil Hall Robert P Hirt T Martin Embley
author_facet	Eva Heinz Tom A Williams Sirintra Nakjang Christophe J Noël Daniel C Swan Alina V Goldberg Simon R Harris Thomas Weinmaier Stephanie Markert Dörte Becher Jörg Bernhardt Tal Dagan Christian Hacker John M Lucocq Thomas Schweder Thomas Rattei Neil Hall Robert P Hirt T Martin Embley
author_sort	Eva Heinz
title	The genome of the obligate intracellular parasite Trachipleistophora hominis: new insights into microsporidian genome dynamics and reductive evolution.
title_short	The genome of the obligate intracellular parasite Trachipleistophora hominis: new insights into microsporidian genome dynamics and reductive evolution.
title_full	The genome of the obligate intracellular parasite Trachipleistophora hominis: new insights into microsporidian genome dynamics and reductive evolution.
title_fullStr	The genome of the obligate intracellular parasite Trachipleistophora hominis: new insights into microsporidian genome dynamics and reductive evolution.
title_full_unstemmed	The genome of the obligate intracellular parasite Trachipleistophora hominis: new insights into microsporidian genome dynamics and reductive evolution.
title_sort	genome of the obligate intracellular parasite trachipleistophora hominis: new insights into microsporidian genome dynamics and reductive evolution.
publisher	Public Library of Science (PLoS)
publishDate	2012
url	https://doaj.org/article/998a2a319a7f43a396865ca1d01f48be
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The genome of the obligate intracellular parasite Trachipleistophora hominis: new insights into microsporidian genome dynamics and reductive evolution.

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