Reduction and expansion inmicrosporidian genome evolution: New insights from comparative genomics

Sirintra Nakjang, Tom A. Williams, Eva Heinz, Andrew K. Watson, Peter G. Foster, Kacper M. Sendra, Sarah E. Heaps, Robert P. Hirt*, T. Martin Embley

*Corresponding author for this work

Research output: Contribution to journalArticle (Academic Journal)peer-review

56 Citations (Scopus)

Abstract

Microsporidia are anabundant 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 micro sporidian genome evolution that have under pinned this success. In this study, weinfer 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 andmetabolism. 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.

Original languageEnglish
Pages (from-to)2285-2303
Number of pages19
JournalGenome Biology and Evolution
Volume5
Issue number12
DOIs
Publication statusPublished - 2013

Keywords

  • Evolution
  • Gene duplication
  • Genome reduction
  • Intracellular parasites
  • Microsporidia
  • Novel gene families

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