The Genome of Spraguea lophii and the Basis of Host-Microsporidian Interactions

Microsporidia are obligate intracellular parasites with the smallest known eukaryotic genomes. Although they are increasingly recognized as economically and medically important parasites, the molecular basis of microsporidian pathogenicity is almost completely unknown and no genetic manipulation sys...

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Main Authors:	Campbell, Scott E., Williams, Tom A., Yousuf, Asim, Soanes, Darren M., Paszkiewicz, Konrad H., Williams, Bryony A. P.
Format:	Online
Language:	English
Published:	Public Library of Science 2013
Online Access:	https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3749934/

id	pubmed-3749934
recordtype	oai_dc
spelling	pubmed-37499342013-08-29 The Genome of Spraguea lophii and the Basis of Host-Microsporidian Interactions Campbell, Scott E. Williams, Tom A. Yousuf, Asim Soanes, Darren M. Paszkiewicz, Konrad H. Williams, Bryony A. P. Research Article Microsporidia are obligate intracellular parasites with the smallest known eukaryotic genomes. Although they are increasingly recognized as economically and medically important parasites, the molecular basis of microsporidian pathogenicity is almost completely unknown and no genetic manipulation system is currently available. The fish-infecting microsporidian Spraguea lophii shows one of the most striking host cell manipulations known for these parasites, converting host nervous tissue into swollen spore factories known as xenomas. In order to investigate the basis of these interactions between microsporidian and host, we sequenced and analyzed the S. lophii genome. Although, like other microsporidia, S. lophii has lost many of the protein families typical of model eukaryotes, we identified a number of gene family expansions including a family of leucine-rich repeat proteins that may represent pathogenicity factors. Building on our comparative genomic analyses, we exploited the large numbers of spores that can be obtained from xenomas to identify potential effector proteins experimentally. We used complex-mix proteomics to identify proteins released by the parasite upon germination, resulting in the first experimental isolation of putative secreted effector proteins in a microsporidian. Many of these proteins are not related to characterized pathogenicity factors or indeed any other sequences from outside the Microsporidia. However, two of the secreted proteins are members of a family of RICIN B-lectin-like proteins broadly conserved across the phylum. These proteins form syntenic clusters arising from tandem duplications in several microsporidian genomes and may represent a novel family of conserved effector proteins. These computational and experimental analyses establish S. lophii as an attractive model system for understanding the evolution of host-parasite interactions in microsporidia and suggest an important role for lineage-specific innovations and fast evolving proteins in the evolution of the parasitic microsporidian lifecycle. Public Library of Science 2013-08-22 /pmc/articles/PMC3749934/ /pubmed/23990793 http://dx.doi.org/10.1371/journal.pgen.1003676 Text en © 2013 Campbell et al http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited.
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	Campbell, Scott E. Williams, Tom A. Yousuf, Asim Soanes, Darren M. Paszkiewicz, Konrad H. Williams, Bryony A. P.
spellingShingle	Campbell, Scott E. Williams, Tom A. Yousuf, Asim Soanes, Darren M. Paszkiewicz, Konrad H. Williams, Bryony A. P. The Genome of Spraguea lophii and the Basis of Host-Microsporidian Interactions
author_facet	Campbell, Scott E. Williams, Tom A. Yousuf, Asim Soanes, Darren M. Paszkiewicz, Konrad H. Williams, Bryony A. P.
author_sort	Campbell, Scott E.
title	The Genome of Spraguea lophii and the Basis of Host-Microsporidian Interactions
title_short	The Genome of Spraguea lophii and the Basis of Host-Microsporidian Interactions
title_full	The Genome of Spraguea lophii and the Basis of Host-Microsporidian Interactions
title_fullStr	The Genome of Spraguea lophii and the Basis of Host-Microsporidian Interactions
title_full_unstemmed	The Genome of Spraguea lophii and the Basis of Host-Microsporidian Interactions
title_sort	genome of spraguea lophii and the basis of host-microsporidian interactions
description	Microsporidia are obligate intracellular parasites with the smallest known eukaryotic genomes. Although they are increasingly recognized as economically and medically important parasites, the molecular basis of microsporidian pathogenicity is almost completely unknown and no genetic manipulation system is currently available. The fish-infecting microsporidian Spraguea lophii shows one of the most striking host cell manipulations known for these parasites, converting host nervous tissue into swollen spore factories known as xenomas. In order to investigate the basis of these interactions between microsporidian and host, we sequenced and analyzed the S. lophii genome. Although, like other microsporidia, S. lophii has lost many of the protein families typical of model eukaryotes, we identified a number of gene family expansions including a family of leucine-rich repeat proteins that may represent pathogenicity factors. Building on our comparative genomic analyses, we exploited the large numbers of spores that can be obtained from xenomas to identify potential effector proteins experimentally. We used complex-mix proteomics to identify proteins released by the parasite upon germination, resulting in the first experimental isolation of putative secreted effector proteins in a microsporidian. Many of these proteins are not related to characterized pathogenicity factors or indeed any other sequences from outside the Microsporidia. However, two of the secreted proteins are members of a family of RICIN B-lectin-like proteins broadly conserved across the phylum. These proteins form syntenic clusters arising from tandem duplications in several microsporidian genomes and may represent a novel family of conserved effector proteins. These computational and experimental analyses establish S. lophii as an attractive model system for understanding the evolution of host-parasite interactions in microsporidia and suggest an important role for lineage-specific innovations and fast evolving proteins in the evolution of the parasitic microsporidian lifecycle.
publisher	Public Library of Science
publishDate	2013
url	https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3749934/
_version_	1612004892482732032

The Genome of Spraguea lophii and the Basis of Host-Microsporidian Interactions

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