The Evolutionary History of Lysine Biosynthesis Pathways Within Eukaryotes

Abstract

Lysine biosynthesis occurs in two ways: the diaminopimelate (DAP) pathway and the α-aminoadipate (AAA) pathway. The former is present in eubacteria, plants, and algae, whereas the latter was understood to be almost exclusive to fungi. The recent finding of the α-aminoadipate reductase (AAR) gene, one of the core genes of the AAA pathway, in the marine protist Corallochytrium limacisporum was, therefore, believed to be a molecular synapomorphy of fungi and C. limacisporum. To test this hypothesis, we undertook a broader search for the AAR gene in eukaryotes, and also analyzed the distribution of the lysA gene, a core gene of the DAP pathway. We show that the evolutionary history of both genes, AAR and lysA, is much more complex than previously believed. Furthermore, the AAR gene is present in several unicellular opisthokonts, thus rebutting the theory that its presence is a molecular synapomorphy between C. limacisporum and fungi. AAR gene seems to be exclusive of Excavata and Unikonts, whereas the lysA gene is present in several unrelated taxa within all major eukaryotic lineages, indicating a role for several lateral gene transfer (LGT) events. Our data imply that the choanoflagellate Monosiga brevicollis and the “choanozoan” Capsaspora owczarzaki acquired their lysA copies from a proteobacterial ancestor. Overall, these observations represent new evidence that the role of LGT in the evolutionary history of eukaryotes may have been more significant than previously thought.

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References

  1. Andersson JO (2005) Lateral gene transfer in eukaryotes. Cell Mol Life Sci 62:1182–1197

    PubMed  Article  CAS  Google Scholar 

  2. Bapteste E, Boucher Y (2008) Lateral gene transfer challenges principles of microbial systematics. Trends Microbiol 16:200–207

    PubMed  Article  CAS  Google Scholar 

  3. Berg JM, Tymoczko JL, Stryer L, Clarke ND (2007) Biochemistry, 6th edn. WH Freeman, New York

    Google Scholar 

  4. Burki F, Shalchian-Tabrizi K, Pawlowski J (2008) Phylogenomics reveals a new ‘megagroup’ including most photosynthetic eukaryotes. Biol Lett 4(4):366–369 Aug 23

    PubMed  Article  Google Scholar 

  5. Cavalier-Smith T (2002) The phagotrophic origin of eukaryotes and phylogenetic classification of Protozoa. Int J Syst Evol Microbiol 52:297–354

    PubMed  CAS  Google Scholar 

  6. Cavalier-Smith T, Chao EE (2003) Phylogeny of choanozoa, apusozoa, and other protozoa and early eukaryote megaevolution. J Mol Evol 56:540–563

    PubMed  Article  CAS  Google Scholar 

  7. Cirillo JD, Weisbrod TR, Banerjee A, Bloom BR, Jacobs WRJ (1994) Genetic determination of the meso-diaminopimelate biosynthetic pathway of mycobacteria. J Bacteriol 176:4424–4429

    PubMed  CAS  Google Scholar 

  8. Doolittle WF, Bapteste E (2007) Pattern pluralism and the Tree of Life hypothesis. Proc Natl Acad Sci USA 104:2043–2049

    PubMed  Article  CAS  Google Scholar 

  9. Eddy SR (1998) Profile hidden Markov models. Bioinformatics 14:755–763

    PubMed  Article  CAS  Google Scholar 

  10. Edgar RC (2004) MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics 5:113

    PubMed  Article  CAS  Google Scholar 

  11. Fahey B, Larroux C, Woodcroft BJ, Degnan BM (2008) Does the high gene density in the sponge NK homeobox gene cluster reflect limited regulatory capacity? Biol Bull 214:205–217

    PubMed  CAS  Article  Google Scholar 

  12. Foerstner KU, Doerks T, Muller J, Raes J, Bork P (2008) A nitrile hydratase in the eukaryote Monosiga brevicollis. PLoS ONE 3:e3976

    PubMed  Article  CAS  Google Scholar 

  13. Garrad RC, Bhattacharjee JK (1992) Lysine biosynthesis in selected pathogenic fungi: characterization of lysine auxotrophs and the cloned LYS1 gene of Candida albicans. J Bacteriol 174:7379–7384

    PubMed  CAS  Google Scholar 

  14. Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704

    PubMed  Article  Google Scholar 

  15. Hampl V, Hug L, Leigh JW, Dacks JB, Lang BF, Simpson AG, Roger AJ (2009) Phylogenomic analyses support the monophyly of Excavata and resolve relationships among eukaryotic “supergroups”. Proc Natl Acad Sci USA 106:3859–3864

    PubMed  Article  Google Scholar 

  16. Hudson AO, Bless C, Macedo P, Chatterjee SP, Singh BK, Gilvarg C, Leustek T (2005) Biosynthesis of lysine in plants: evidence for a variant of the known bacterial pathways. Biochim Biophys Acta 1721:27–36

    PubMed  CAS  Google Scholar 

  17. Hutton CA, Perugini MA, Gerrard JA (2007) Inhibition of lysine biosynthesis: an evolving antibiotic strategy. Mol Biosyst 3:458–465

    PubMed  Article  CAS  Google Scholar 

  18. Keeling PJ, Palmer JD (2008) Horizontal gene transfer in eukaryotic evolution. Nat Rev Genet 9(8):605–618 Aug

    PubMed  Article  CAS  Google Scholar 

  19. King N, Westbrook MJ, Young SL, Kuo A, Abedin M, Chapman J, Fairclough S, Hellsten U, Isogai Y, Letunic I, Marr M, Pincus D, Putnam N, Rokas A, Wright KJ, Zuzow R, Dirks W, Good M, Goodstein D, Lemons D, Li W, Lyons JB, Morris A, Nichols S, Richter DJ, Salamov A, Sequencing JG, Bork P, Lim WA, Manning G, Miller WT, McGinnis W, Shapiro H, Tjian R, Grigoriev IV, Rokhsar D (2008) The genome of the choanoflagellate Monosiga brevicollis and the origin of metazoans. Nature 451:783–788

    PubMed  Article  CAS  Google Scholar 

  20. McInerney JO, Cotton JA, Pisani D (2008) The prokaryotic tree of life: past, present. and future? Trends Ecol Evol 23:276–281

    PubMed  Article  Google Scholar 

  21. Mendoza L, Taylor JW, Ajello L (2002) The class mesomycetozoea: a heterogeneous group of microorganisms at the animal-fungal boundary. Annu Rev Microbiol 56:315–344

    PubMed  Article  CAS  Google Scholar 

  22. Minge MA, Silberman JD, Orr RJ, Cavalier-Smith T, Shalchian-Tabrizi K, Burki F, Skjaeveland A, Jakobsen KS (2008) Evolutionary position of breviate amoebae and the primary eukaryote divergence. Proc Biol Sci 276:597–604

    Article  CAS  Google Scholar 

  23. Miyazaki T, Miyazaki J, Yamane H, Nishiyama M (2004) alpha-Aminoadipate aminotransferase from an extremely thermophilic bacterium, Thermus thermophilus. Microbiology 150:2327–2334

    PubMed  Article  CAS  Google Scholar 

  24. Moya A, Pereto J, Gil R, Latorre A (2008) Learning how to live together: genomic insights into prokaryote-animal symbioses. Nat Rev Genet 9:218–229

    PubMed  Article  CAS  Google Scholar 

  25. Nowack EC, Melkonian M, Glockner G (2008) Chromatophore genome sequence of Paulinella sheds light on acquisition of photosynthesis by eukaryotes. Curr Biol 18:410–418

    PubMed  Article  CAS  Google Scholar 

  26. Putnam NH, Srivastava M, Hellsten U, Dirks B, Chapman J, Salamov A, Terry A, Shapiro H, Lindquist E, Kapitonov VV, Jurka J, Genikhovich G, Grigoriev IV, Lucas SM, Steele RE, Finnerty JR, Technau U, Martindale MQ, Rokhsar DS (2007) Sea anemone genome reveals ancestral eumetazoan gene repertoire and genomic organization. Science 317:86–94

    PubMed  Article  CAS  Google Scholar 

  27. Ruiz-Trillo I, Lane CE, Archibald JM, Roger AJ (2006) Insights into the evolutionary origin and genome architecture of the unicellular opisthokonts Capsaspora owczarzaki and Sphaeroforma arctica. J Eukaryot Microbiol 53(5):379–384

    PubMed  Article  CAS  Google Scholar 

  28. Ruiz-Trillo I, Burger G, Holland PW, King N, Lang BF, Roger AJ, Gray MW (2007) The origins of multicellularity: a multi-taxon genome initiative. Trends Genet 23:113–118

    PubMed  Article  CAS  Google Scholar 

  29. Ruiz-Trillo I, Roger AJ, Burger G, Gray MW, Lang BF (2008) A phylogenomic investigation into the origin of metazoa. Mol Biol Evol 25:664–672

    PubMed  Article  CAS  Google Scholar 

  30. Shalchian-Tabrizi K, Minge MA, Espelund M, Orr R, Ruden T, Jakobsen KS, Cavalier-Smith T (2008) Multigene phylogeny of choanozoa and the origin of animals. PLoS ONE 3:e2098

    PubMed  Article  CAS  Google Scholar 

  31. Simpson AG, Inagaki Y, Roger AJ (2005) Comprehensive Multi-Gene Phylogenies of Excavate Protists Reveal the Evolutionary Positions of ‘Primitive’ Eukaryotes. Mol Biol Evol 23:615–625

    PubMed  Article  CAS  Google Scholar 

  32. Soria-Carrasco V, Castresana J (2008) Estimation of phylogenetic inconsistencies in the three domains of life. Mol Biol Evol 25:2319–2329

    PubMed  Article  CAS  Google Scholar 

  33. Srivastava M, Begovic E, Chapman J, Putnam NH, Hellsten U, Kawashima T, Kuo A, Mitros T, Salamov A, Carpenter ML, Signorovitch AY, Moreno MA, Kamm K, Grimwood J, Schmutz J, Shapiro H, Grigoriev IV, Buss LW, Schierwater B, Dellaporta SL, Rokhsar DS (2008) The Trichoplax genome and the nature of placozoans. Nature 454:955–960

    PubMed  Article  CAS  Google Scholar 

  34. Stamatakis A (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:2688–2690

    PubMed  Article  CAS  Google Scholar 

  35. Stamatakis A, Ludwig T, Meier H (2005) RAxML-III: a fast program for maximum likelihood-based inference of large phylogenetic trees. Bioinformatics 21:456–463

    PubMed  Article  CAS  Google Scholar 

  36. Steenkamp ET, Wright J, Baldauf SL (2006) The protistan origins of animals and fungi. Mol Biol Evol 23:93–106

    PubMed  Article  CAS  Google Scholar 

  37. Sumathi JC, Raghukumar S, Kasbekar DP, Raghukumar C (2006) Molecular evidence of fungal signatures in the marine protist Corallochytrium limacisporum and its implications in the evolution of animals and fungi. Protist 157:363–376

    PubMed  Article  CAS  Google Scholar 

  38. Tyler BM, Tripathy S, Zhang X, Dehal P, Jiang RH, Aerts A, Arredondo FD, Baxter L, Bensasson D, Beynon JL, Chapman J, Damasceno CM, Dorrance AE, Dou D, Dickerman AW, Dubchak IL, Garbelotto M, Gijzen M, Gordon SG, Govers F, Grunwald NJ, Huang W, Ivors KL, Jones RW, Kamoun S, Krampis K, Lamour KH, Lee MK, McDonald WH, Medina M, Meijer HJ, Nordberg EK, Maclean DJ, Ospina-Giraldo MD, Morris PF, Phuntumart V, Putnam NH, Rash S, Rose JK, Sakihama Y, Salamov AA, Savidor A, Scheuring CF, Smith BM, Sobral BW, Terry A, Torto-Alalibo TA, Win J, Xu Z, Zhang H, Grigoriev IV, Rokhsar DS, Boore JL (2006) Phytophthora genome sequences uncover evolutionary origins and mechanisms of pathogenesis. Science 313:1261–1266

    PubMed  Article  CAS  Google Scholar 

  39. Velasco AM, Leguina JI, Lazcano A (2002) Molecular evolution of the lysine biosynthetic pathways. J Mol Evol 55:445–459

    PubMed  Article  CAS  Google Scholar 

  40. Vogel HJ (1965) Lysine biosynthesis and evolution. In: Bryson V (ed) Handbook of evolving genes and proteins, 5th edn. Academic Press, New York, pp 25–40

  41. Watkins RF, Gray MW (2006) The frequency of eubacterium-to-eukaryote lateral gene transfers shows significant cross-taxa variation within amoebozoa. J Mol Evol 63:801–814

    PubMed  Article  CAS  Google Scholar 

  42. Watkins RF, Gray MW (2008) Sampling gene diversity across the supergroup Amoebozoa: large EST data sets from Acanthamoeba castellanii, Hartmannella vermiformis, Physarum polycephalum, Hyperamoeba dachnaya and Hyperamoeba sp.. Protist 159:269–281

    PubMed  Article  Google Scholar 

  43. Xu H, Andi B, Qian J, West AH, Cook PF (2006) The α-aminoadipate pathway for lysine biosynthesis in fungi. Cell Biochem and Biophys 46:43–64

    Article  CAS  Google Scholar 

  44. Zientz E, Dandekar T, Gross R (2004) Metabolic interdependence of obligate intracellular bacteria and their insect hosts. Microbiol Mol Biol Rev 68:745–770

    PubMed  Article  CAS  Google Scholar 

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Acknowledgments

Thanks to bioportal and to Andrew J. Roger for providing access to their computer resources. We thank Kamran Shalchian-Tabrizi for providing us with the sequence of Ministeria vibrans and Bernard Degnan for accession to the Amphimedon proteome data. We also thank Eric Bapteste, Tom Cavalier-Smith and Franz Lang for helpful insights. We also thank Roser Rotchés for her support. This work was supported by an ICREA contract and an ERC Starting Grant to IR-T, as well as a Grant BFU2006-06003 from MEC to JP.

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Correspondence to Iñaki Ruiz-Trillo.

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Torruella, G., Suga, H., Riutort, M. et al. The Evolutionary History of Lysine Biosynthesis Pathways Within Eukaryotes. J Mol Evol 69, 240–248 (2009). https://doi.org/10.1007/s00239-009-9266-x

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Keywords

  • Lysine biosynthesis
  • Molecular evolution
  • Corallochytrium
  • Opisthokonts
  • AAR gene
  • lysA gene
  • Lateral gene transfer