Skip to main content

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.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

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]

    CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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]

    Article  CAS  PubMed  Google Scholar 

  • Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39(4):783–791

    Article  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Gabaldon T, Huynen MA (2003) Reconstruction of the proto-mitochondrial metabolism. Science 301(5633):609. doi:10.1126/science.1085463; 301/5633/609 [pii]

    Article  CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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]

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Hawksworth DL (1991) The fungal dimension of biodiversity: magnitude, significance, and conservation. Mycol Res 95(4):641–655

    Article  Google Scholar 

  • 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]

    Article  CAS  PubMed  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • 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

    Google Scholar 

  • 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]

    CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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]

    CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Mueller G, Schmit J (2007) Fungal biodiversity: what do we know? What can we predict? Biodivers Conserv 16:1–5

    Article  Google Scholar 

  • Ohno S (1970) Evolution by gene duplication. Springer, New York

    Google Scholar 

  • 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]

    Article  CAS  PubMed  Google Scholar 

  • Schmit J, Mueller G (2007) An estimate of the lower limit of global fungal diversity. Biodivers Conserv 16(1):99–111

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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]

    Article  PubMed  Google Scholar 

  • 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]

    Article  CAS  PubMed  Google Scholar 

  • Visser W, Scheffers WA, Batenburg-van der Vegte WH, van Dijken JP (1990) Oxygen requirements of yeasts. Appl Environ Microbiol 56(12):3785–3792

    CAS  PubMed  Google Scholar 

  • 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]

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

Download references

Acknowledgment

TG and MMH are founded through a grant of the Spanish Ministry of Science (BFV2009-09168).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Marina Marcet-Houben .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2011 Springer-Verlag Berlin Heidelberg

About this chapter

Cite this chapter

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

Download citation

Publish with us

Policies and ethics