Gain and loss of multiple functionally related, horizontally transferred genes in the reduced genomes of two microsporidian parasites

Edited by David M. Hillis, University of Texas, Austin, TX, and approved June 25, 2012 (received for review March 26, 2012)
July 16, 2012
109 (31) 12638-12643

Abstract

Microsporidia of the genus Encephalitozoon are widespread pathogens of animals that harbor the smallest known nuclear genomes. Complete sequences from Encephalitozoon intestinalis (2.3 Mbp) and Encephalitozoon cuniculi (2.9 Mbp) revealed massive gene losses and reduction of intergenic regions as factors leading to their drastically reduced genome size. However, microsporidian genomes also have gained genes through horizontal gene transfers (HGT), a process that could allow the parasites to exploit their hosts more fully. Here, we describe the complete sequences of two intermediate-sized genomes (2.5 Mbp), from Encephalitozoon hellem and Encephalitozoon romaleae. Overall, the E. hellem and E. romaleae genomes are strikingly similar to those of Encephalitozoon cuniculi and Encephalitozoon intestinalis in both form and content. However, in addition to the expected expansions and contractions of known gene families in subtelomeric regions, both species also were found to harbor a number of protein-coding genes that are not found in any other microsporidian. All these genes are functionally related to the metabolism of folate and purines but appear to have originated by several independent HGT events from different eukaryotic and prokaryotic donors. Surprisingly, the genes are all intact in E. hellem, but in E. romaleae those involved in de novo synthesis of folate are all pseudogenes. Overall, these data suggest that a recent common ancestor of E. hellem and E. romaleae assembled a complete metabolic pathway from multiple independent HGT events and that one descendent already is dispensing with much of this new functionality, highlighting the transient nature of transferred genes.

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Data Availability

Data deposition: The sequences reported in this paper have been deposited in the GenBank database, www.ncbi.nlm.nih.gov/genbank/ [accession nos. CP002713–CP002724 (Encephalitozoon hellem) and CP003518–CP003530 (Encephalitozoon romaleae)].

Acknowledgments

We thank N. Fast for kindly giving us access to the E. cuniculi 5′Race dataset and C. Grisdale for verifying the splicing of the new introns. This work was supported by Grant MOP-42517 from the Canadian Institute for Health Research (to P.J.K.), a Discovery Grant from the Natural Sciences and Engineering Council of Canada (to N.C.), and Grant AI31788 from the National Institute of Allergy and Infectious Diseases of the National Institutes of Health (to L.M.W.). J.-F.P. was supported by a Fonds Québécois de la Recherche sur la Nature et les Technologies/Génome Québec Louis-Berlinguet postdoctoral fellowship. F.B. was supported by a prospective researcher postdoctoral fellowship from Swiss National Science Foundation and by a grant to the Centre for Microbial Diversity and Evolution from the Tula Foundation. P.J.K. and N.C. are a Fellow and a Scholar, respectively, of the Canadian Institute for Advanced Research.

Supporting Information

Supporting Information (PDF)
Supporting Information
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Supporting Information
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Information & Authors

Information

Published in

Go to Proceedings of the National Academy of Sciences
Proceedings of the National Academy of Sciences
Vol. 109 | No. 31
July 31, 2012
PubMed: 22802648

Classifications

Data Availability

Data deposition: The sequences reported in this paper have been deposited in the GenBank database, www.ncbi.nlm.nih.gov/genbank/ [accession nos. CP002713–CP002724 (Encephalitozoon hellem) and CP003518–CP003530 (Encephalitozoon romaleae)].

Submission history

Published online: July 16, 2012
Published in issue: July 31, 2012

Keywords

  1. evolution
  2. genomics
  3. parasitology

Acknowledgments

We thank N. Fast for kindly giving us access to the E. cuniculi 5′Race dataset and C. Grisdale for verifying the splicing of the new introns. This work was supported by Grant MOP-42517 from the Canadian Institute for Health Research (to P.J.K.), a Discovery Grant from the Natural Sciences and Engineering Council of Canada (to N.C.), and Grant AI31788 from the National Institute of Allergy and Infectious Diseases of the National Institutes of Health (to L.M.W.). J.-F.P. was supported by a Fonds Québécois de la Recherche sur la Nature et les Technologies/Génome Québec Louis-Berlinguet postdoctoral fellowship. F.B. was supported by a prospective researcher postdoctoral fellowship from Swiss National Science Foundation and by a grant to the Centre for Microbial Diversity and Evolution from the Tula Foundation. P.J.K. and N.C. are a Fellow and a Scholar, respectively, of the Canadian Institute for Advanced Research.

Notes

This article is a PNAS Direct Submission.

Authors

Affiliations

Jean-François Pombert1
Department of Botany, Canadian Institute for Advanced Research, University of British Columbia, Vancouver, BC, V6T 1Z4 Canada;
Mohammed Selman1
Department of Biology, Canadian Institute for Advanced Research, University of Ottawa, Ottawa, ON, K1N 1H7 Canada;
Fabien Burki
Department of Botany, Canadian Institute for Advanced Research, University of British Columbia, Vancouver, BC, V6T 1Z4 Canada;
Floyd T. Bardell
Department of Botany, Canadian Institute for Advanced Research, University of British Columbia, Vancouver, BC, V6T 1Z4 Canada;
Laurent Farinelli
Fasteris SA, CH-1228 Plan-les-Ouates, Geneva, Switzerland;
Leellen F. Solter
Illinois Natural History Survey, Prairie Research Institute, University of Illinois, Champaign, IL 61820;
Douglas W. Whitman
School of Biological Sciences, Illinois State University, Normal, IL 61790; and
Louis M. Weiss
Division of Parasitology, Department of Pathology, and
Division of Infectious Diseases, Department of Medicine, Albert Einstein College of Medicine, Bronx, NY 10461
Nicolas Corradi2 [email protected]
Department of Biology, Canadian Institute for Advanced Research, University of Ottawa, Ottawa, ON, K1N 1H7 Canada;
Patrick J. Keeling2 [email protected]
Department of Botany, Canadian Institute for Advanced Research, University of British Columbia, Vancouver, BC, V6T 1Z4 Canada;

Notes

2
To whom correspondence may be addressed. E-mail: [email protected] or [email protected].
Author contributions: J.-F.P., N.C., and P.J.K. designed research; J.-F.P., M.S., F.B., L.F., and N.C. performed research; L.F.S., D.W.W., and L.M.W. contributed new reagents/analytic tools; J.-F.P., M.S., F.B., F.T.B., N.C., and P.J.K. analyzed data; and J.-F.P., N.C., and P.J.K. wrote the paper.
1
J.-F.P. and M.S. contributed equally to this work.

Competing Interests

The authors declare no conflict of interest.

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    Gain and loss of multiple functionally related, horizontally transferred genes in the reduced genomes of two microsporidian parasites
    Proceedings of the National Academy of Sciences
    • Vol. 109
    • No. 31
    • pp. 12261-12835

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