A recent whole-genome duplication divides populations of a globally-distributed microsporidian
Molecular Biology and Evolution
Oxford University Press (OUP)
© The Author 2016. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/, which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.
The Microsporidia are a major group of intracellular fungi and important parasites of animals including insects, fish, and immunocompromised humans. Microsporidian genomes have undergone extreme reductive evolution but there are major differences in genome size and structure within the group: some are prokaryote-like in size and organisation (<3 Mb of gene-dense sequence) whilst others have more typically eukaryotic genome architectures. To gain fine-scale, population-level insight into the evolutionary dynamics of these tiny eukaryotic genomes, we performed the broadest microsporidian population genomic study to date, sequencing geographically isolated strains of Spraguea, a marine microsporidian infecting goosefish worldwide. Our analysis revealed that population structure across the Atlantic Ocean is associated with a conserved difference in ploidy, with American and Canadian isolates sharing an ancestral whole genome duplication that was followed by widespread pseudogenisation and sorting-out of paralogue pairs. Whilst past analyses have suggested de novo gene formation of microsporidian-specific genes, we found evidence for the origin of new genes from noncoding sequence since the divergence of these populations. Some of these genes experience selective constraint, suggesting the evolution of new functions and local host adaptation. Combining our data with published microsporidian genomes, we show that nucleotide composition across the phylum is shaped by a mutational bias favouring A and T nucleotides, which is opposed by an evolutionary force favouring an increase in genomic GC content. This work reveals ongoing dramatic reorganisation of genome structure and the evolution of new gene functions in modern microsporidians despite extensive genomic streamlining in their common ancestor.
The authors would like to thank John Brookfield and David Studholme for helpful discussions. This work was supported by a Marie Curie Intra-European postdoctoral fellowship (T.A.W.) and the European Research Council Advanced Investigator Programme and the Wellcome Trust (grant numbers ERC- 2010- AdG-268701 045404 to T.M.E.) It is also supported by a Royal Society University Research Fellowship (B.A.P.W.).
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Vol. 33 (8), pp. 2002-2015