Reduction and Expansion in Microsporidian Genome Evolution: New Insights from Comparative Genomics

Microsporidia are an abundant group of obligate intracellular parasites of other eukaryotes, including immunocompromised humans, but the molecular basis of their intracellular lifestyle and pathobiology are poorly understood. New genomes from a taxonomically broad range of microsporidians, complemen...

Full description

Bibliographic Details
Main Authors:	Nakjang, Sirintra, Williams, Tom A., Heinz, Eva, Watson, Andrew K., Foster, Peter G., Sendra, Kacper M., Heaps, Sarah E., Hirt, Robert P., Martin Embley, T.
Format:	Online
Language:	English
Published:	Oxford University Press 2013
Online Access:	https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3879972/

id	pubmed-3879972
recordtype	oai_dc
spelling	pubmed-38799722014-01-03 Reduction and Expansion in Microsporidian Genome Evolution: New Insights from Comparative Genomics Nakjang, Sirintra Williams, Tom A. Heinz, Eva Watson, Andrew K. Foster, Peter G. Sendra, Kacper M. Heaps, Sarah E. Hirt, Robert P. Martin Embley, T. Research Article Microsporidia are an abundant group of obligate intracellular parasites of other eukaryotes, including immunocompromised humans, but the molecular basis of their intracellular lifestyle and pathobiology are poorly understood. New genomes from a taxonomically broad range of microsporidians, complemented by published expression data, provide an opportunity for comparative analyses to identify conserved and lineage-specific patterns of microsporidian genome evolution that have underpinned this success. In this study, we infer that a dramatic bottleneck in the last common microsporidian ancestor (LCMA) left a small conserved core of genes that was subsequently embellished by gene family expansion driven by gene acquisition in different lineages. Novel expressed protein families represent a substantial fraction of sequenced microsporidian genomes and are significantly enriched for signals consistent with secretion or membrane location. Further evidence of selection is inferred from the gain and reciprocal loss of functional domains between paralogous genes, for example, affecting transport proteins. Gene expansions among transporter families preferentially affect those that are located on the plasma membrane of model organisms, consistent with recruitment to plug conserved gaps in microsporidian biosynthesis and metabolism. Core microsporidian genes shared with other eukaryotes are enriched in orthologs that, in yeast, are highly expressed, highly connected, and often essential, consistent with strong negative selection against further reduction of the conserved gene set since the LCMA. Our study reveals that microsporidian genome evolution is a highly dynamic process that has balanced constraint, reductive evolution, and genome expansion during adaptation to an extraordinarily successful obligate intracellular lifestyle. Oxford University Press 2013 2013-11-19 /pmc/articles/PMC3879972/ /pubmed/24259309 http://dx.doi.org/10.1093/gbe/evt184 Text en © The Author(s) 2013. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. http://creativecommons.org/licenses/by/3.0/ This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/3.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.
repository_type	Open Access Journal
institution_category	Foreign Institution
institution	US National Center for Biotechnology Information
building	NCBI PubMed
collection	Online Access
language	English
format	Online
author	Nakjang, Sirintra Williams, Tom A. Heinz, Eva Watson, Andrew K. Foster, Peter G. Sendra, Kacper M. Heaps, Sarah E. Hirt, Robert P. Martin Embley, T.
spellingShingle	Nakjang, Sirintra Williams, Tom A. Heinz, Eva Watson, Andrew K. Foster, Peter G. Sendra, Kacper M. Heaps, Sarah E. Hirt, Robert P. Martin Embley, T. Reduction and Expansion in Microsporidian Genome Evolution: New Insights from Comparative Genomics
author_facet	Nakjang, Sirintra Williams, Tom A. Heinz, Eva Watson, Andrew K. Foster, Peter G. Sendra, Kacper M. Heaps, Sarah E. Hirt, Robert P. Martin Embley, T.
author_sort	Nakjang, Sirintra
title	Reduction and Expansion in Microsporidian Genome Evolution: New Insights from Comparative Genomics
title_short	Reduction and Expansion in Microsporidian Genome Evolution: New Insights from Comparative Genomics
title_full	Reduction and Expansion in Microsporidian Genome Evolution: New Insights from Comparative Genomics
title_fullStr	Reduction and Expansion in Microsporidian Genome Evolution: New Insights from Comparative Genomics
title_full_unstemmed	Reduction and Expansion in Microsporidian Genome Evolution: New Insights from Comparative Genomics
title_sort	reduction and expansion in microsporidian genome evolution: new insights from comparative genomics
description	Microsporidia are an abundant group of obligate intracellular parasites of other eukaryotes, including immunocompromised humans, but the molecular basis of their intracellular lifestyle and pathobiology are poorly understood. New genomes from a taxonomically broad range of microsporidians, complemented by published expression data, provide an opportunity for comparative analyses to identify conserved and lineage-specific patterns of microsporidian genome evolution that have underpinned this success. In this study, we infer that a dramatic bottleneck in the last common microsporidian ancestor (LCMA) left a small conserved core of genes that was subsequently embellished by gene family expansion driven by gene acquisition in different lineages. Novel expressed protein families represent a substantial fraction of sequenced microsporidian genomes and are significantly enriched for signals consistent with secretion or membrane location. Further evidence of selection is inferred from the gain and reciprocal loss of functional domains between paralogous genes, for example, affecting transport proteins. Gene expansions among transporter families preferentially affect those that are located on the plasma membrane of model organisms, consistent with recruitment to plug conserved gaps in microsporidian biosynthesis and metabolism. Core microsporidian genes shared with other eukaryotes are enriched in orthologs that, in yeast, are highly expressed, highly connected, and often essential, consistent with strong negative selection against further reduction of the conserved gene set since the LCMA. Our study reveals that microsporidian genome evolution is a highly dynamic process that has balanced constraint, reductive evolution, and genome expansion during adaptation to an extraordinarily successful obligate intracellular lifestyle.
publisher	Oxford University Press
publishDate	2013
url	https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3879972/
_version_	1612043996880699392

Reduction and Expansion in Microsporidian Genome Evolution: New Insights from Comparative Genomics

Similar Items