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

Nakjang, Sirintra and Williams, Tom A. and Heinz, Eva and Watson, Andrew K. and Foster, Peter G. and Sendra, Kacper M. and Heaps, Sarah E. and Hirt, Robert P. and Embley, T. Martin (2013) Reduction and expansion inmicrosporidian genome evolution : new insights from comparative genomics. Genome Biology and Evolution, 5 (12). pp. 2285-2303. ISSN 1759-6653 (https://doi.org/10.1093/gbe/evt184)

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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.

ORCID iDs

Nakjang, Sirintra, Williams, Tom A., Heinz, Eva ORCID logoORCID: https://orcid.org/0000-0003-4413-3756, Watson, Andrew K., Foster, Peter G., Sendra, Kacper M., Heaps, Sarah E., Hirt, Robert P. and Embley, T. Martin;