Organelles that illuminate the origins of Trichomonas hydrogenosomes and Giardia mitosomes

Abstract

Many anaerobic microbial parasites possess highly modified mitochondria known as mitochondrion-related organelles (MROs). The best-studied of these are the hydrogenosomes of Trichomonas vaginalis and Spironucleus salmonicida, which produce ATP anaerobically through substrate-level phosphorylation with concomitant hydrogen production; and the mitosomes of Giardia intestinalis, which are functionally reduced and lack any role in ATP production. However, to understand the metabolic specializations that these MROs underwent in adaptation to parasitism, data from their free-living relatives are needed. Here, we present a large-scale comparative transcriptomic study of MROs across a major eukaryotic group, Metamonada, examining lineage-specific gain and loss of metabolic functions in the MROs of Trichomonas, Giardia, Spironucleus and their free-living relatives. Our analyses uncover a complex history of ATP production machinery in diplomonads such as Giardia, and their closest relative, Dysnectes; and a correlation between the glycine cleavage machinery and lifestyles. Our data further suggest the existence of a previously undescribed biochemical class of MRO that generates hydrogen but is incapable of ATP synthesis.

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Figure 1: Phylogeny of Metamonada and distribution of MRO-localizing proteins.
Figure 2: Predicted mitochondrial protein import proteins in metamonads.
Figure 3: Evolutionary transitions of metabolic pathways of MROs from the common ancestor of Parabasalia and Fornicata to representative extant species.

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Acknowledgements

M.K., M.M.L. and C.W.S. were supported by a grant (MOP-142349) from the Canadian Institutes of Health Research awarded to A.J.R. This work was also supported, in part, by a grant from the JSPS Strategic Young Researcher Overseas Visits Program (awarded to R.K.), by NSERC Grant 298366-2009 to A.G.B.S., by a Czech Science Foundation grant to I.Č. (project GA14-14105S) and by grants from the Japan Society for the Promotion of Science (JSPS; nos 15H05606 and 15K14591 awarded to R.K., 23117005 and 15H05231 awarded to T.H., and 23117006 awarded to Y.I.). We thank A. A. Heiss for his help with Trimastix marina data generation, and N. Ros for her comments on the manuscript.

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M.K., R.K., J.O.A., Y.I., A.G.B.S., T.H. and A.J.R. conceived and designed the experiments; M.K., K.K., I.Č., J.D.S., F.X., A.Y. and Q.Z. performed the experiments; M.M.L., M.K., R.K., C.W.S., K.K., L.E. and Y.I. analysed the data; R.K., C.W.S., J.D.S., K.T., Y.I., A.G.B.S., T.H. and A.J.R. contributed materials and/or analysis tools; and M.M.L., M.K., R.K., A.G.B.S. and A.J.R. wrote the paper.

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Correspondence to Tetsuo Hashimoto or Andrew J. Roger.

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Supplementary information

Supplementary Information

Supplementary Figures 1–20, Supplementary Table 1 (PDF 1444 kb)

Supplementary Data 1

Predicted mitochondrion-related organelle proteins, and selected predicted cytosolic proteins, in metamonads. (XLSX 149 kb)

Supplementary Data 2

File containing the raw phylogenetic trees depicted in Supplementary Figs 4–20, including bootstrap support values, in Newick format. (TXT 539 kb)

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Leger, M., Kolisko, M., Kamikawa, R. et al. Organelles that illuminate the origins of Trichomonas hydrogenosomes and Giardia mitosomes. Nat Ecol Evol 1, 0092 (2017). https://doi.org/10.1038/s41559-017-0092

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