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A mitochondrial Hsp70 orthologue in Vairimorpha necatrix : molecular evidence that microsporidia once contained mitochondria

1997; Elsevier BV; Volume: 7; Issue: 12 Linguagem: Inglês

10.1016/s0960-9822(06)00420-9

1879-0445

Robert P. Hirt, Bryan Healy, Charles R. Vossbrinck, Elizabeth U. Canning, T. Martin Embley,

Vector-borne infectious diseases

Microsporidia are small (1–20 μm) obligate intracellular parasites of a variety of eukaryotes, and they are serious opportunistic pathogens of immunocompromised patients [[1]Canning EU Hollister WS Human infections with microsporidia.Rev Med Microbiol. 1992; 3: 35-42Google Scholar]. Microsporidia are often assigned to the first branch in gene trees of eukaryotes [2Vossbrinck CR Maddox JV Friedman S Debrunner-Vossbrinck BA Woese CR Ribosomal RNA sequence suggests microsporidia are extremely ancient eukaryotes.Nature. 1987; 326 (87172991): 411-414Crossref PubMed Scopus (422) Google Scholar, 3Kamaishi T Hashimoto T Nakamura Y Masuda Y Nakamura F Okamoto K-I Complete nucleotide sequences of the gene encoding translation elongation factor EF-1 alpha and 2 from a microsporidian parasite, Glugea plecoglossi: implications for the deepest branching of eukaryotes.J Biochem. 1996; 120: 1095-1103Crossref PubMed Scopus (55) Google Scholar], and are reported to lack mitochondria [2Vossbrinck CR Maddox JV Friedman S Debrunner-Vossbrinck BA Woese CR Ribosomal RNA sequence suggests microsporidia are extremely ancient eukaryotes.Nature. 1987; 326 (87172991): 411-414Crossref PubMed Scopus (422) Google Scholar, 4Cavalier-Smith T Eukaryotes with no mitochondria.Nature. 1987; 326: 332Crossref PubMed Scopus (258) Google Scholar]. Like diplomonads and trichomonads, microsporidia are hypothesised to have diverged from the main eukaryotic stock prior to the event that led to the mitochondrion endosymbiosis [2Vossbrinck CR Maddox JV Friedman S Debrunner-Vossbrinck BA Woese CR Ribosomal RNA sequence suggests microsporidia are extremely ancient eukaryotes.Nature. 1987; 326 (87172991): 411-414Crossref PubMed Scopus (422) Google Scholar, 4Cavalier-Smith T Eukaryotes with no mitochondria.Nature. 1987; 326: 332Crossref PubMed Scopus (258) Google Scholar]. They have thus assumed importance as putative relics of premitochondrion eukaryote evolution. Recent data have now revealed that diplomonads and trichomonads contain genes that probably originated from the mitochondrion endosymbiont [5Keeling PJ Doolittle WF Evidence that eukaryotic triose phosphate isomerase is of alpha-proteobacterial origin.Proc Natl Acad Sci USA. 1997; 94 (97188457): 1270-1275Crossref PubMed Scopus (92) Google Scholar, 6Horner DS Hirt RP Kilvington S Lloyd D Embley TM Molecular data suggest an early acquisition of the mitochondrion endosymbiont.Proc R Soc Lond B. 1996; 263: 1053-1059Crossref PubMed Scopus (129) Google Scholar, 7Germot A Philippe H LeGuyader H Presence of a mitochondrial-type 70-kDa heat shock protein in Trichomonas vaginalis suggest a very early mitochondrial endosymbiosis in eukaryotes.Proc Natl Acad Sci USA. 1996; 93 (97121435): 14614-14617Crossref PubMed Scopus (159) Google Scholar, 8Bui ETN Bradley PJ Johnson PJ A common evolutionary origin for mitochondria and hydrogenosomes.Proc Natl Acad Sci USA. 1996; 93 (96382521): 9651-9656Crossref PubMed Scopus (220) Google Scholar, 9Roger AJ Clark AJ Doolittle WF A possible mitochondrial gene in the early-branching amitochondriate protist Trichomonas vaginalis.Proc Natl Acad Sci USA. 1996; 93 (97121436): 14618-14622Crossref PubMed Scopus (132) Google Scholar], leaving microsporidia as chief candidates for an extant primitively amitochondriate eukaryote group. We have now identified a gene in the microsporidium Vairimorpha necatrix that appears to be orthologous to the eukaryotic (symbiont-derived) Hsp70 gene, the protein product of which normally functions in mitochondria. The simplest interpretation of our data is that microporidia have lost mitochondria while retaining genetic evidence of their past presence. This strongly suggests that microsporidia are not primitively amitochondriate and makes feasible an evolutionary scenario whereby all extant eukaryotes share a common ancestor which contained mitochondria.