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

Jean François Pombert, Mohammed Selman, Fabien Burki, Floyd T. Bardell, Laurent Farinelli, Leellen F. Solter, Douglas W. Whitman, Louis M. Weiss, Nicolas Corradi, Patrick J. Keeling

Research output: Contribution to journalArticle

58 Citations (Scopus)

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.

Original languageEnglish (US)
Pages (from-to)12638-12643
Number of pages6
JournalProceedings of the National Academy of Sciences of the United States of America
Volume109
Issue number31
DOIs
StatePublished - Jul 31 2012

Fingerprint

Encephalitozoon
Parasites
Genome
Horizontal Gene Transfer
Encephalitozoon cuniculi
Genes
Folic Acid
Microsporidia
Genome Size
Purines
Pseudogenes
Intergenic DNA
Metabolic Networks and Pathways
Proteins

Keywords

  • Evolution
  • Genomics
  • Parasitology

ASJC Scopus subject areas

  • General

Cite this

Gain and loss of multiple functionally related, horizontally transferred genes in the reduced genomes of two microsporidian parasites. / Pombert, Jean François; Selman, Mohammed; Burki, Fabien; Bardell, Floyd T.; Farinelli, Laurent; Solter, Leellen F.; Whitman, Douglas W.; Weiss, Louis M.; Corradi, Nicolas; Keeling, Patrick J.

In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 109, No. 31, 31.07.2012, p. 12638-12643.

Research output: Contribution to journalArticle

Pombert, Jean François ; Selman, Mohammed ; Burki, Fabien ; Bardell, Floyd T. ; Farinelli, Laurent ; Solter, Leellen F. ; Whitman, Douglas W. ; Weiss, Louis M. ; Corradi, Nicolas ; Keeling, Patrick J. / Gain and loss of multiple functionally related, horizontally transferred genes in the reduced genomes of two microsporidian parasites. In: Proceedings of the National Academy of Sciences of the United States of America. 2012 ; Vol. 109, No. 31. pp. 12638-12643.
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