The tangled past of eukaryotic enzymes involved in anaerobic metabolism
Status PubMed-not-MEDLINE Jazyk angličtina Země Spojené státy americké Médium print
Typ dokumentu časopisecké články
PubMed
22016847
PubMed Central
PMC3190275
DOI
10.4161/mge.1.1.15588
PII: 2159-2543-1-1-9
Knihovny.cz E-zdroje
- Publikační typ
- časopisecké články MeSH
There is little doubt that genes can spread across unrelated prokaryotes, eukaryotes and even between these domains. It is expected that organisms inhabiting a common niche may exchange their genes even more often due to their physical proximity and similar demands. One such niche is anaerobic or microaerophilic environments in some sediments and intestines of animals. Indeed, enzymes advantageous for metabolism in these environments often exhibit an evolutionary history incoherent with the history of their hosts indicating potential transfers. The evolutionary paths of some very basic enzymes for energy metabolism of anaerobic eukaryotes (pyruvate formate lyase, pyruvate:ferredoxin oxidoreductase, [FeFe]hydrogenase and arginine deiminase) seems to be particularly intriguing and although their histories are not identical they share several unexpected features in common. Every enzyme mentioned above is present in groups of eukaryotes that are unrelated to each other. Although the enzyme phylogenies are not always robustly supported, they always suggest that the eukaryotic homologues form one or two clades, in which the relationships are not congruent with the eukaryotic phylogeny. Finally, these eukaryotic enzymes are never specifically related to homologues from α-proteobacteria, ancestors of mitochondria. The most plausible explanation for evolution of this pattern expects one or two interdomain transfers to one or two eukaryotes from prokaryotes, who were not the mitochondrial endosymbiont. Once the genes were introduced into the eukaryotic domain they have spread to other eukaryotic groups exclusively via eukaryote-to-eukaryote transfers. Currently, eukaryote-to-eukaryote gene transfers have been regarded as less common than prokaryote-to-eukaryote transfers. The fact that eukaryotes accepted genes for these enzymes solely from other eukaryotes and not prokaryotes present in the same environment is surprising.
Zobrazit více v PubMed
Keeling PJ, Palmer JD. Horizontal gene transfer in eukaryotic evolution. Nat Rev Genet. 2008;9:605–618. doi: 10.1038/nrg2386. PubMed DOI
Andersson JO. Lateral gene transfer in eukaryotes. Cell Mol Life Sci. 62:1182–1197. doi: 10.1007/s00018-005-4539-z. PubMed DOI PMC
Richards TA, Dacks JB, Jenkinson JM, Thornton CR, Talbot NJ. Evolution of filamentous plant pathogens: gene exchange across eukaryotic kingdoms. Curr Biol. 2006;16:1857–1864. doi: 10.1016/j.cub.2006.07.052. PubMed DOI
Whitaker JW, McConkey GA, Westhead DR. The transferome of metabolic genes explored: analysis of the horizontal transfer of enzyme encoding genes in unicellular eukaryotes. Genome Biol. 2009;10:36. doi: 10.1186/gb-2009-10-4-r36. PubMed DOI PMC
Martin W, Schnarrenberger C. The evolution of the Calvin cycle from prokaryotic to eukaryotic chromosomes: a case study of functional redundancy in ancient pathways through endosymbiosis. Curr Genet. 1997;32:1–18. doi: 10.1007/s002940050241. PubMed DOI
Doolittle WF. You are what you eat: a gene transfer ratchet could account for bacterial genes in eukaryotic nuclear genomes. Trends Genet. 1998;14:307–311. doi: 10.1016/S0168-9525(98)01494-2. PubMed DOI
Yap WH, Zhang Z, Wang Y. Distinct types of rRNA operons exist in the genome of the actinomycete Thermomonospora chromogena and evidence for horizontal transfer of an entire rRNA operon. J Bacteriol. 1999;181:5201–5209. PubMed PMC
Miller SR, Augustine S, Olson TL, Blankenship RE, Selker J, Wood AM. Discovery of a free-living chlorophyll d-producing cyanobacterium with a hybrid proteobacterial/cyanobacterial small-subunit rRNA gene. Proc Natl Acad Sci USA. 2005;102:850–855. doi: 10.1073/pnas.0405667102. PubMed DOI PMC
Cohen O, Gophna U, Pupko T. The complexity hypothesis revisited: connectivity rather than function constitutes a barrier to horizontal gene transfer. Mol Biol Evol. 2011;28:1481–1489. doi: 10.1093/molbev/msq333. PubMed DOI
Rivera MC, Jain R, Moore JE, Lake JA. Genomic evidence for two functionally distinct gene classes. Proc Natl Acad Sci USA. 1998;95:6239–6244. PubMed PMC
Andersson JO. Genome evolution of anaerobic protists: metabolic adaptation via gene acquisition. In: LA Katz, D Bhattacharya., editors. Genomics and Evolution of Microbial Eukaryotes. Oxford: Oxford Univ Press; 2006. pp. 109–122.
Slot JC, Rokas A. Horizontal transfer of a large and highly toxic secondary metabolic gene cluster between Fungi. Curr Biol. 2011;21:134–139. doi: 10.1016/j.cub.2010.12.020. PubMed DOI
Zhaxybayeva O. Detection and quantitative assessment of horizontal gene transfer. In: Gogarten MB, Gogarten JP, Olendzenki L, editors. Horisontal gene transfer. New York: Humana Press; 2009. pp. 195–213. PubMed DOI
Stairs CW, Roger AJ, Hampl V. Eukaryotic pyruvate formate lyase and its activating enzyme were acquired laterally from a firmicute. Mol Biol Evol. 2011 doi: 10.1093/molbev/msr032. PubMed DOI
Atteia A, et al. Pyruvate formate-lyase and a novel route of eukaryotic ATP synthesis in Chlamydomonas mitochondria. J Biol Chem. 2006;281:9909–9918. doi: 10.1074/jbc.M507862200. PubMed DOI
Susko E. First-order correct bootstrap support adjustments for splits that allow hypothesis testing when using maximum likelihood estimation. Mol Biol Evol. 2010;27:1621–1629. doi: 10.1093/molbev/msq048. PubMed DOI
Martin W, Müller M. The hydrogen hypothesis for the first eukaryote. Nature. 1998;392:37–41. doi: 10.1038/32096. PubMed DOI
Moreira D, Lopez-Garcia P. Symbiosis between methanogenic archaea and delta-proteobacteria as the origin of eukaryotes: the syntrophic hypothesis. J Mol Evol. 1998;47:517–530. doi: 10.1007/PL00006408. PubMed DOI
Karlberg O, Canbäck B, Kurland CG, Andersson SGE. The Dual Origin of the Yeast Mitochondrial Proteome. Yeast. 2000;17:170–187. doi: 10.1002/1097-0061(20000930)17:3 < 170::AID-YEA25 > 3.0.CO;2-V. PubMed DOI PMC
Kurland CG, Andersson SGE. Origin and Evolution of the Mitochondrial Proteome. Microbiol Mol Biol Rev. 2000;64:4786–4820. PubMed PMC
Gabaldón T, Huynen MA. Reconstruction of the Proto-Mitochondrial Metabolism. Science. 2003;301:609. doi: 10.1126/science.1085463. PubMed DOI
Touz MC, et al. Arginine deiminase has multiple regulatory rols in the biology of Giardia lamblia. J Cell Sci. 2008;121:2930–2938. doi: 10.1242/jcs.026963. PubMed DOI PMC
Morada M, et al. Hydrogenosome-localization of arginine deiminase in Trichomonas vaginalis. Mol Biochem Parasitol. 2011;176:51–54. doi: 10.1016/j.molbiopara.2010.10.004. PubMed DOI PMC
Hug LA, Stechmann A, Roger AJ. Phylogenetic distributions and histories of proteins involved in anaerobic pyruvate metabolism in eukaryotes. Mol Biol Evol. 2010;27:311–324. doi: 10.1093/molbev/msp237. PubMed DOI
Barton RM, Worman HJ. Prenylated prelamin A interacts with Narf, a novel nuclear protein. J Biol Chem. 1999;274:30008–30018. doi: 10.1074/jbc.274.42.30008. PubMed DOI
Liapounova NA, Hampl V, Gordon PM, Sensen CW, Gedamu L, Dacks JB. Reconstructing the mosaic glycolytic pathway of the anaerobic eukaryote Monocercomonoides. Eukaryot Cell. 2006;5:2138–2146. doi: 10.1128/EC.00258-06. PubMed DOI PMC
Stechmann A, Baumgartner M, Silberman JD, Roger AJ. The glycolytic pathway of Trimastix pyriformis is an evolutionary mosaic. BMC Evol Biol. 2006;23:6–101. doi: 10.1186/1471-2148-6-101. PubMed DOI PMC
Stamatakis A. RAxML-VI-HPC: Maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics. 2006;22:2688–2690. doi: 10.1093/bioinformatics/btl446. PubMed DOI
Le SQ, Gascuel O. An improved general amino acid replacement matrix. Mol Biol Evol. 2008;25:1307–1320. doi: 10.1093/molbev/msn067. PubMed DOI