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Microsporidia Evolved from Ancestral Sexual Fungi

2008; Elsevier BV; Volume: 18; Issue: 21 Linguagem: Inglês

10.1016/j.cub.2008.09.030

1879-0445

Soo Chan Lee, Nicolas Corradi, Edmond J. Byrnes, Santiago Torres‐Martínez, Fred S. Dietrich, Patrick J. Keeling, Joseph Heitman,

Chromosomal and Genetic Variations

Microsporidia are obligate, intracellular eukaryotic pathogens that infect animal cells, including humans [1Keeling P.J. Fast N.M. Microsporidia: Biology and evolution of highly reduced intracellular parasites.Annu. Rev. Microbiol. 2002; 56: 93-116Crossref PubMed Scopus (357) Google Scholar]. Previous studies suggested microsporidia share a common ancestor with fungi [2Edlind T.D. Li J. Visvesvara G.S. Vodkin M.H. McLaughlin G.L. Katiyar S.K. Phylogenetic analysis of beta-tubulin sequences from amitochondrial protozoa.Mol. Phylogenet. Evol. 1996; 5: 359-367Crossref PubMed Scopus (185) Google Scholar, 3Keeling P.J. Doolittle W.F. Alpha-tubulin from early-diverging eukaryotic lineages and the evolution of the tubulin family.Mol. Biol. Evol. 1996; 13: 1297-1305Crossref PubMed Scopus (250) Google Scholar, 4Keeling P.J. Congruent evidence from alpha-tubulin and beta-tubulin gene phylogenies for a zygomycete origin of microsporidia.Fungal Genet. Biol. 2003; 38: 298-309Crossref PubMed Scopus (178) Google Scholar, 5James T.Y. Kauff F. Schoch C.L. Matheny P.B. Hofstetter V. Cox C.J. Celio G. Gueidan C. Fraker E. Miadlikowska J. et al.Reconstructing the early evolution of Fungi using a six-gene phylogeny.Nature. 2006; 443: 818-822Crossref PubMed Scopus (1264) Google Scholar, 6Hirt R.P. Logsdon J.M. Healy B. Dorey M.W. Doolittle W.F. Embley T.M. Microsporidia are related to Fungi: Evidence from the largest subunit of RNA polymerase II and other proteins.Proc. Natl. Acad. Sci. USA. 1999; 96: 580-585Crossref PubMed Scopus (411) Google Scholar, 7Gill E.E. Fast N.M. Assessing the microsporidia-fungi relationship: Combined phylogenetic analysis of eight genes.Gene. 2006; 375: 103-109Crossref PubMed Scopus (86) Google Scholar]. However, the exact nature of this phylogenetic relationship is unclear because of unusual features of microsporidial genomes, which are compact with fewer and highly divergent genes [8Thomarat F. Vivarès C.P. Gouy M. Phylogenetic analysis of the complete genome sequence of Encephalitozoon cuniculi supports the fungal origin of microsporidia and reveals a high frequency of fast-evolving genes.J. Mol. Evol. 2004; 59: 780-791Crossref PubMed Scopus (109) Google Scholar]. As a consequence, it is unclear whether microsporidia evolved from a specific fungal lineage, or whether microsporidia are a sister group to all fungi. Here, we present evidence addressing this controversial question that is independent of sequence-based phylogenetic reconstruction, but rather based on genome structure. In the zygomycete basal fungal lineage, the sex locus is a syntenic gene cluster governing sexual reproduction in which a high mobility group (HMG) transcription-factor gene is flanked by triose-phosphate transporter (TPT) and RNA helicase genes [9Idnurm A. Walton F.J. Floyd A. Heitman J. Identification of the sex genes in an early diverged fungus.Nature. 2008; 451: 193-196Crossref PubMed Scopus (112) Google Scholar]. Strikingly, microsporidian genomes harbor a sex-related locus with the same genes in the same order. Genome-wide synteny analysis reveals multiple other loci conserved between microsporidia and zygomycetes to the exclusion of all other fungal lineages with sequenced genomes. These findings support the hypothesis that microsporidia are true fungi that descended from a zygomycete ancestor and suggest microsporidia may have an extant sexual cycle.