Abstract
The oxidative phosphorylation (OXPHOS) pathway plays a central role in the energetic metabolism of aerobic organisms. Despite such centrality, this pathway has not remained unaltered through evolution, and variations of it, including its complete loss, can be found in organisms adapted to different ecological niches. Fungi, a eukaryotic group of species with a high metabolic diversity, represent an ideal phylum in which to study the evolutionary plasticity of the OXPHOS pathway from a phylogenomics perspective. With more than 100 completely sequenced genomes, and thanks to recent progress in elucidating their evolutionary relationships, fungal species have served to reveal the evolutionary mechanisms that underlie the evolution of the core respiratory pathways. In this chapter, we review recent progress toward the characterization of OXPHOS components in fungi and in understanding their evolution. A special focus is devoted to the history of duplications that the multi-protein complexes in OXPHOS have experienced.
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References
Abdrakhmanova A, Zickermann V, Bostina M, Radermacher M, Schagger H, Kerscher S, Brandt U (2004) Subunit composition of mitochondrial complex I from the yeast Yarrowia lipolytica. Biochim Biophys Acta 1658(1–2):148–156. doi:10.1016/j.bbabio.2004.04.019; S0005272804001446 [pii]
Anisimova M, Gascuel O (2006) Approximate likelihood-ratio test for branches: a fast, accurate, and powerful alternative. Syst Biol 55(4):539–552. doi:T808388N86673K61 [pii]; 10.1080/10635150600755453
Burri L, Williams BA, Bursac D, Lithgow T, Keeling PJ (2006) Microsporidian mitosomes retain elements of the general mitochondrial targeting system. Proc Natl Acad Sci USA 103(43):15916–15920. doi:0604109103 [pii]; 10.1073/pnas.0604109103
Cardol P, Gonzalez-Halphen D, Reyes-Prieto A, Baurain D, Matagne RF, Remacle C (2005) The mitochondrial oxidative phosphorylation proteome of Chlamydomonas reinhardtii deduced from the Genome Sequencing Project. Plant Physiol 137(2):447–459. doi:137/2/447 [pii]; 10.1104/pp. 104.054148
Delsuc F, Brinkmann H, Philippe H (2005) Phylogenomics and the reconstruction of the tree of life. Nat Rev Genet 6(5):361–375. doi: nrg1603 [pii]; 10.1038/nrg1603
Dobrynin K, Abdrakhmanova A, Richers S, Hunte C, Kerscher S, Brandt U (2010) Characterization of two different acyl carrier proteins in complex I from Yarrowia lipolytica. Biochim Biophys Acta 1797(2):152–159. doi:S0005-2728(09)00263-1 [pii]; 10.1016/j.bbabio.2009.09.007
Duarte M, Peters M, Schulte U, Videira A (2003) The internal alternative NADH dehydrogenase of Neurospora crassa mitochondria. Biochem J 371(Pt 3):1005–1011. doi:10.1042/BJ20021374; BJ20021374 [pii]
Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39(4):783–791
Fitzpatrick DA, Logue ME, Stajich JE, Butler G (2006) A fungal phylogeny based on 42 complete genomes derived from supertree and combined gene analysis. BMC Evol Biol 6:99. doi:1471-2148-6-99 [pii]; 10.1186/1471-2148-6-99
Gabaldon T, Huynen MA (2003) Reconstruction of the proto-mitochondrial metabolism. Science 301(5633):609. doi:10.1126/science.1085463; 301/5633/609 [pii]
Gabaldon T, Huynen MA (2004) Shaping the mitochondrial proteome. Biochim Biophys Acta 1659(2–3):212–220. doi:S0005-2728(04)00248-8 [pii]; 10.1016/j.bbabio.2004.07.011
Gabaldon T, Rainey D, Huynen MA (2005) Tracing the evolution of a large protein complex in the eukaryotes, NADH:ubiquinone oxidoreductase (complex I). J Mol Biol 348(4):857–870. doi:S0022-2836(05)00237-8 [pii]; 10.1016/j.jmb.2005.02.067
Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52(5):696–704. doi:54QHX07WB5K5XCX4 [pii]
Hackstein JH, Tjaden J, Huynen M (2006) Mitochondria, hydrogenosomes and mitosomes: products of evolutionary tinkering! Curr Genet 50(4):225–245. doi:10.1007/s00294-006-0088-8
Hawksworth DL (1991) The fungal dimension of biodiversity: magnitude, significance, and conservation. Mycol Res 95(4):641–655
Helmerhorst EJ, Murphy MP, Troxler RF, Oppenheim FG (2002) Characterization of the mitochondrial respiratory pathways in Candida albicans. Biochim Biophys Acta 1556(1):73–80. doi:S0005272802003080 [pii]
Huerta-Cepas J, Dopazo H, Dopazo J, Gabaldon T (2007) The human phylome. Genome Biol 8(6):R109. doi:gb-2007-8-6-r109 [pii]; 10.1186/gb-2007-8-6-r109
Huerta-Cepas J, Capella-Gutierrez S, Pryszcz LP, Denisov I, Kormes D, Marcet-Houben M, Gabaldon T (2010) PhylomeDB v3.0: an expanding repository of genome-wide collections of trees, alignments and phylogeny-based orthology and paralogy predictions. Nucleic Acids Res. doi:doi:gkq1109 [pii]; 10.1093/nar/gkq1109
Joseph-Horne T, Hollomon DW, Wood PM (2001) Fungal respiration: a fusion of standard and alternative components. Biochim Biophys Acta 1504(2–3):179–195. doi:S0005272800002516 [pii]
Keeling PJ, Corradi N, Morrison HG, Haag KL, Ebert D, Weiss LM, Akiyoshi DE, Tzipori S (2010) The reduced genome of the parasitic microsporidian Enterocytozoon bieneusi lacks genes for core carbon metabolism. Genome Biol Evol 2:304–309. doi:evq022 [pii]; 10.1093/gbe/evq022
Kerscher SJ (2000) Diversity and origin of alternative NADH:ubiquinone oxidoreductases. Biochim Biophys Acta 1459(2–3):274–283. doi:S0005-2728(00)00162-6 [pii]
Lavin JL, Oguiza JA, Ramirez L, Pisabarro AG (2008) Comparative genomics of the oxidative phosphorylation system in fungi. Fungal Genet Biol 45(9):1248–1256. doi:S1087-1845(08)00108-4 [pii]; 10.1016/j.fgb.2008.06.005
Letunic I, Bork P (2007) Interactive Tree Of Life (iTOL): an online tool for phylogenetic tree display and annotation. Bioinformatics 23(1):127–128. doi:btl529 [pii]; 10.1093/bioinformatics/btl529
Li Q, Bai Z, O’Donnell A, Harvey LM, Hoskisson PA, McNeil B (2010) Oxidative stress in fungal fermentation processes: the roles of alternative respiration. Biotechnol Lett. doi:10.1007/s10529-010-0471-x
Ma LJ, Ibrahim AS, Skory C, Grabherr MG, Burger G, Butler M, Elias M, Idnurm A, Lang BF, Sone T, Abe A, Calvo SE, Corrochano LM, Engels R, Fu J, Hansberg W, Kim JM, Kodira CD, Koehrsen MJ, Liu B, Miranda-Saavedra D, O’Leary S, Ortiz-Castellanos L, Poulter R, Rodriguez-Romero J, Ruiz-Herrera J, Shen YQ, Zeng Q, Galagan J, Birren BW, Cuomo CA, Wickes BL (2009) Genomic analysis of the basal lineage fungus Rhizopus oryzae reveals a whole-genome duplication. PLoS Genet 5(7):e1000549. doi:10.1371/journal.pgen.1000549
Magnani T, Soriani FM, Martins Vde P, Policarpo AC, Sorgi CA, Faccioli LH, Curti C, Uyemura SA (2008) Silencing of mitochondrial alternative oxidase gene of Aspergillus fumigatus enhances reactive oxygen species production and killing of the fungus by macrophages. J Bioenerg Biomembr 40(6):631–636. doi:10.1007/s10863-008-9191-5
Marcet-Houben M, Gabaldon T (2009) The tree versus the forest: the fungal tree of life and the topological diversity within the yeast phylome. PLoS ONE 4(2):e4357. doi:10.1371/journal.pone.0004357
Marcet-Houben M, Marceddu G, Gabaldon T (2009) Phylogenomics of the oxidative phosphorylation in fungi reveals extensive gene duplication followed by functional divergence. BMC Evol Biol 9:295. doi:1471-2148-9-295 [pii]; 10.1186/1471-2148-9-295
Marella M, Seo BB, Yagi T, Matsuno-Yagi A (2009) Parkinson’s disease and mitochondrial complex I: a perspective on the Ndi1 therapy. J Bioenerg Biomembr 41(6):493–497. doi:10.1007/s10863-009-9249-z
Mueller G, Schmit J (2007) Fungal biodiversity: what do we know? What can we predict? Biodivers Conserv 16:1–5
Ohno S (1970) Evolution by gene duplication. Springer, New York
Papp B, Pal C, Hurst LD (2003) Dosage sensitivity and the evolution of gene families in yeast. Nature 424(6945):194–197. doi:10.1038/nature01771; nature01771 [pii]
Schmit J, Mueller G (2007) An estimate of the lower limit of global fungal diversity. Biodivers Conserv 16(1):99–111
Snel B, Huynen MA, Dutilh BE (2005) Genome trees and the nature of genome evolution. Annu Rev Microbiol 59:191–209. doi:10.1146/annurev.micro.59.030804.121233
Suvase SA, Annapure US, Singhal RS (2010) Gellan gum as an immobilization matrix for the production of cyclosporin A. J Microbiol Biotechnol 20(7):1086–1091. doi:JMB020-07-05 [pii]
Takaya N (2009) Response to hypoxia, reduction of electron acceptors, and subsequent survival by filamentous fungi. Biosci Biotechnol Biochem 73(1):1–8. doi:JST.JSTAGE/bbb/80487 [pii]
Visser W, Scheffers WA, Batenburg-van der Vegte WH, van Dijken JP (1990) Oxygen requirements of yeasts. Appl Environ Microbiol 56(12):3785–3792
Voncken F, Boxma B, Tjaden J, Akhmanova A, Huynen M, Verbeek F, Tielens AG, Haferkamp I, Neuhaus HE, Vogels G, Veenhuis M, Hackstein JH (2002) Multiple origins of hydrogenosomes: functional and phylogenetic evidence from the ADP/ATP carrier of the anaerobic chytrid Neocallimastix sp. Mol Microbiol 44(6):1441–1454. doi:2959 [pii]
Wang H, Xu Z, Gao L, Hao B (2009) A fungal phylogeny based on 82 complete genomes using the composition vector method. BMC Evol Biol 9:195. doi:1471-2148-9-195 [pii]; 10.1186/1471-2148-9-195
Williams BA, Elliot C, Burri L, Kido Y, Kita K, Moore AL, Keeling PJ (2010) A broad distribution of the alternative oxidase in microsporidian parasites. PLoS Pathog 6(2):e1000761. doi:10.1371/journal.ppat.1000761
Wittig I, Carrozzo R, Santorelli FM, Schagger H (2006) Supercomplexes and subcomplexes of mitochondrial oxidative phosphorylation. Biochim Biophys Acta 1757(9–10):1066–1072. doi:S0005-2728(06)00130-7 [pii]; 10.1016/j.bbabio.2006.05.006
Wolf YI, Rogozin IB, Grishin NV, Tatusov RL, Koonin EV (2001) Genome trees constructed using five different approaches suggest new major bacterial clades. BMC Evol Biol 1:8
Yagi T, Seo BB, Nakamaru-Ogiso E, Marella M, Barber-Singh J, Yamashita T, Matsuno-Yagi A (2006) Possibility of transkingdom gene therapy for complex I diseases. Biochim Biophys Acta 1757(5–6):708–714. doi:S0005-2728(06)00024-7 [pii]; 10.1016/j.bbabio.2006.01.011
Acknowledgment
TG and MMH are founded through a grant of the Spanish Ministry of Science (BFV2009-09168).
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Marcet-Houben, M., Gabaldón, T. (2011). Evolution of Fungi and Their Respiratory Metabolism. In: Pontarotti, P. (eds) Evolutionary Biology – Concepts, Biodiversity, Macroevolution and Genome Evolution. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-20763-1_15
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DOI: https://doi.org/10.1007/978-3-642-20763-1_15
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