An Ectosymbiosis-Based Mechanism of Eukaryogenesis

Main Article Content

Tze-Fei Wong Chung-Kwon Chan Xi Long Xue Hong

Abstract

The mechanisms proposed for eukaryogenesis are divisible into mitochondria-early and mitochondria-late ones, where the mitochondriate-eukaryotes were evolutionary precursors or products of the amitochondriate-eukaryotes respectively. Analysis of prokaryote-to-eukaryote gene transfers in eukaryogenesis showed two tranches of high-intensity transfers from prokaryotes to eukaryotes mediated by the endosymbioses that gave rise to mitochondria and chloroplasts, and hundreds of medium-intensity transfers which included the transfer of hydrogenase and pyruvate: ferredoxin oxidoreductase genes from the Thermoanaerobacter-Hungateiclostridium-Sporanaerobacter group of bacteria to the amitochondriate eukaryotes. Since 94.5% of these medium-intensity transfers generated more than 100 inter-proteome similarity hits between each donor-recipient pair, they were not readily explicable by horizontal gene transfers or endosymbioses, pointing instead to the participation of a huge number of ectosymbiotic transfers. The euryarchaeon Aciduliprofundum boonei and the gammaproteobacterium Escherichia coli were among the foremost contributors of archaeal and bacterial genes to the eukaryotic DNA-apparati respectively, and the ratios of the genes in different eukaryotes indicated that Microsporidia have retained more of the genomic imprint of Aciduliprofundum than all other eukaryotes. These findings supported an ectosymbiosis-based mechanism of eukaryogenesis with Aciduliprofundum as the Archaeal Parent of Eukarya, and Microsporidia as the eukaryotes phylogenetically closest to the Last Eukaryotic Common Ancestor.

Keywords: Aciduliprofundum, archaeal parent, ectosymbiosis, endosymbiosis, eukaryogenesis, valyl-tRNA synthetase

Article Details

How to Cite
WONG, Tze-Fei et al. An Ectosymbiosis-Based Mechanism of Eukaryogenesis. Medical Research Archives, [S.l.], v. 11, n. 1, jan. 2023. ISSN 2375-1924. Available at: <https://esmed.org/MRA/mra/article/view/3365>. Date accessed: 25 apr. 2024. doi: https://doi.org/10.18103/mra.v11i1.3365.
Section
Research Articles

References

1. Martin WF, Garg S, Zimorski V. Endosymbiotic theories for eukaryote origin. Phil Trans Roy Soc London B Biol Sci. 2015; 370: 20140330. doi: 10.1098/rstb.2014.0330.

2. Cavalier-Smith T. The origin of eukaryotic and archaebacterial cells. Ann N Y Acad Sci. 1987;503:17-54. doi:10.1111/j.1749-6632.1987.tb40596.x.

3. Searcy DG, Stein DB, Searcy KB. A mycoplasma-like archaebacterium possibly related to the nucleus and cytoplasms of eukaryotic cells. Ann N Y Acad Sci 1981;361:312-324. doi:10.1111/j.1749-6632.1981.tb46527.x.

4. Cox CJ, Foster PG, Hirt RP, Harris SR, Embley TM. The archaebacterial origin of eukaryotes. Proc Natl Acad Sci U S A 2008;105(51):20356-20361. doi:10.1073/pnas.0810647105.

5. Martin W, Müller M. The hydrogen hypothesis for the first eukaryote. Nature 1998;392(6671):37-41. doi:10.1038/32096.

6. 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(5):517-530. doi:10.1007/pl00006408

7. Margulis L, Dolan MF, Guerrero R. The chimeric eukaryote: origin of the nucleus from the karyomastigont in amitochondriate protists. Proc Natl Acad Sci U S A 2000;97(13):6954-6959. doi:10.1073/pnas.97.13.6954.

8. Long X, Xue H, Wong JTF. Descent of bacteria and eukarya from an archaeal root of life. Evol Bioinform Online 2020;16:1176934320908267. Published 2020 Jun 23. doi:10.1177/1176934320908267.

9. Hartman H, Fedorov A. The origin of the eukaryotic cell: a genomic investigation. Proc Natl Acad Sci U S A 2002;99(3):1420-1425. doi:10.1073/pnas.032658599.

10. Eme L, Spang A, Lombard J, Stairs CW, Ettema TJG. Archaea and the origin of eukaryotes. Nat Rev Microbiol 2018;16(2):120. doi:10.1038/nrmicro.2017.154.

11. Raymann K, Brochier-Armanet C, Gribaldo S. The two-domain tree of life is linked to a new root for the Archaea. Proc Natl Acad Sci U S A 2015;112(21):6670-6675. doi:10.1073/pnas.1420858112.

12. Cotton JA, McInerney JO. Eukaryotic genes of archaebacterial origin are more important than the more numerous eubacterial genes, irrespective of function. Proc Natl Acad Sci U S A 2010;107(40):17252-17255. doi:10.1073/pnas.1000265107.

13. Vossbrinck CR, Maddox JV, Friedman S, Debrunner-Vossbrinck BA, Woese CR. Ribosomal RNA sequence suggests microsporidia are extremely ancient eukaryotes. Nature 1987;326(6111):411-414. doi:10.1038/326411a0.

14. Sogin ML, Silberman JD. Evolution of the protists and protistan parasites from the perspective of molecular systematics. Int J Parasitol 1998;28(1):11-20. doi:10.1016/s0020-7519(97)00181-1.

15. Kamaishi T, Hashimoto T, Nakamura Y, et al. Protein phylogeny of translation elongation factor EF-1 alpha suggests microsporidians are extremely ancient eukaryotes. J Mol Evol 1996;42(2):257-263. doi:10.1007/BF02198852.

16. Pittis AA, Gabaldón T. Late acquisition of mitochondria by a host with chimaeric prokaryotic ancestry. Nature 2016;531(7592):101-104. doi:10.1038/nature16941.

17. Horner DS, Hirt RP, Kilvington S, Lloyd D, Embley TM. Molecular data suggest an early acquisition of the mitochondrion endosymbiont. Proc Biol Sci 1996;263(1373):1053-1059. doi:10.1098/rspb.1996.0155.

18. Roger AJ. Reconstructing early events in eukaryotic evolution. Am Nat 1999;154(S4):S146-S163. doi:10.1086/303290.

19. Van de Peer Y, Ben Ali A, Meyer A. Microsporidia: accumulating molecular evidence that a group of amitochondriate and suspectedly primitive eukaryotes are just curious fungi. Gene 2000;246(1-2):1-8. doi:10.1016/s0378-1119(00)00063-9.

20. Arisue N, Sánchez LB, Weiss LM, Müller M, Hashimoto T. Mitochondrial-type hsp70 genes of the amitochondriate protists Giardia intestinalis, Entamoeba histolytica and two microsporidians. Parasitol Int 2002;51(1):9-16. doi:10.1016/s1383-5769(01)00093-9.

21. de Graaf RM, Duarte I, van Alen TA, et al. The hydrogenosomes of Psalteriomonas lanterna. BMC Evol Biol. 2009;9:287. Published 2009 Dec 9. doi:10.1186/1471-2148-9-287

22. Degli Esposti M. Late mitochondrial acquisition, Really? Genome Biol Evol 2016;8(6):2031-2035. doi:10.1093/gbe/evw130.

23. Martin WF, Roettger M, Ku C, Garg SG, Nelson-Sathi S, Landan G. Late mitochondrial origin is an artifact. Genome Biol Evol 2017;9(2):373-379. doi:10.1093/gbe/evx027.

24. Gray MW. The pre-endosymbiont hypothesis: a new perspective on the origin and evolution of mitochondria. Cold Spring Harb Perspect Biol 2014;6(3):a016097. Published 2014 Mar 1. doi:10.1101/cshperspect.a016097.

25. Esser C, Ahmadinejad N, Wiegand C, Rotte C, Sebastiani F, Gelius-Dietrich G, Henze K, Kretschmann E, Richly E, Leister D, et al. A genome phylogeny for mitochondria among alpha-proteobacteria and a predominantly eubacterial ancestry of yeast nuclear genes. Mol Biol Evol 2004; 21: 1643-1660. doi: 10.1093/molbev/msh160.

26. Rochette NC, Brochier-Armanet C, Gouy M. Phylogenomic test of the hypotheses for the evolutionary origin of eukaryotes. Mol Biol Evol 2014; 31: 832-845. doi: 10.1093/molbev/mst27.

27. Blanchard JL, Lynch M. Organellar genes: why do they end up in the nucleus?. Trends Genet 2000;16(7):315-320. doi:10.1016/s0168-9525(00)02053-9.

28. Clark K, Karsch-Mizrachi I, Lipman DJ, Ostell J, W. Sayers E, et al. GenBank. Nucleic Acids Res. 2016; 44 D67-72. doi: 10.1093/nar/gkv127.

29. O'Leary NA, Wright MW, Brister JR, Ciufo S, Haddad D, et al. Reference sequence (RefSeq) database at NCBI: current status, taxonomic expansion, and functional annotation. Nucl Acid Res. 2016; 44: D733-745. doi: 10.1093/nar/gkv1189.

30. Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J, Bealer K, Madden TL. BLAST+: architecture and applications. BMC Bioinform. 2009; 10: 421. doi: 10.1186/1471-2105-10-421.

31. Enderlin CS, Meeks JC. Pure culture and reconstitution of the Anthoceros-Nostoc symbiotic association. Planta. 1983; 158: 157-165. Doi: 10.1007/BF00397709.

32. Hétérier V, David B, De Ridder C, Rigaud T. Ectosymbiosis is a critical factor in the local benthic biodiversity of the Antarctic deep sea. Mar Ecol Prog Ser. Published online 2008. doi:10.3354/meps07487.

33. Noda S, Ohkuma M, Yamada A, Hongoh Y, Kudo T. Phylogenetic position and in situ identification of ectosymbiotic spirochetes on protists in the termite gut. Appl Environ Microbiol. 2003;69(1):625-633. doi:10.1128/AEM.69.1.625-633.2003.

34. Golyshina OV, Toshchakov SV, Makarova KS, et al. 'ARMAN' archaea depend on association with euryarchaeal host in culture and in situ. Nat Commun. 2017;8(1):60. Published 2017 Jul 5. doi:10.1038/s41467-017-00104-7.

35. Bauermeister J, Ramette A, Dattagupta S. Repeatedly evolved host-specific ectosymbioses between sulfur-oxidizing bacteria and amphipods living in a cave ecosystem. PLoS One. 2012;7(11):e50254. doi:10.1371/journal.pone.0050254.

36. Tatusov RL, Galperin MY, Natale DA, Koonin EV. The COG database: a tool for genome-scale analysis of protein functions and evolution. Nucleic Acids Res. 2000;28(1):33-36. doi:10.1093/nar/28.1.33.

37. Andersson SG, Kurland CG. Origins of mitochondria and hydrogenosomes. Curr Opin Microbiol. 1999;2(5):535-541. doi:10.1016/s1369-5274(99)00013-2.
38. Abhishek A, Bavishi A, Bavishi A, Choudhary M. Bacterial genome chimaerism and the origin of mitochondria. Can J Microbiol. 2011;57(1):49-61. doi:10.1139/w10-099.

39. Wu B, Buljic A, Hao W. Extensive horizontal transfer and homologous recombination generate highly chimeric mitochondrial genomes in Yeast. Mol Biol Evol. 2015;32(10):2559-2570. doi:10.1093/molbev/msv127.

40. Ku C, Nelson-Sathi S, Roettger M, Garg S, Hazkani-Covo E, Martin WF. Endosymbiotic gene transfer from prokaryotic pangenomes: Inherited chimerism in eukaryotes. Proc Natl Acad Sci U S A. 2015;112(33):10139-10146. doi:10.1073/pnas.1421385112.

41. Martijn J, Vosseberg J, Guy L, Offre P, Ettema TJG. Deep mitochondrial origin outside the sampled alphaproteobacteria. Nature. 2018;557(7703):101-105. doi:10.1038/s41586-018-0059-5.

42. Whatley JM, John P, Whatley FR. From extracellular to intracellular: the establishment of mitochondria and chloroplasts. Proc R Soc Lond B Biol Sci. 1979;204(1155):165-187. doi:10.1098/rspb.1979.0020.

43. Horner DS, Hirt RP, Embley TM. A single eubacterial origin of eukaryotic pyruvate: ferredoxin oxidoreductase genes: implications for the evolution of anaerobic eukaryotes. Mol Biol Evol. 1999;16(9):1280-1291. doi:10.1093/oxfordjournals.molbev.a026218.

44. Tielens AG, Rotte C, van Hellemond JJ, Martin W. Mitochondria as we don't know them. Trends Biochem Sci. 2002;27(11):564-572. doi:10.1016/s0968-0004(02)02193-x.

45. Hirt RP, Logsdon JM Jr, Healy B, Dorey MW, Doolittle WF, Embley TM. Microsporidia are related to Fungi: evidence from the largest subunit of RNA polymerase II and other proteins. Proc Natl Acad Sci U S A. 1999;96(2):580-585. doi:10.1073/pnas.96.2.580.

46. Keeling PJ. Congruent evidence from α-tubulin and β-tubulin gene phylogenies for a zygomycete origin of Microsporidia. Fungal Genet Biol. 2003: 298-309. doi:10.1016/S1087-1845(02)00537-6.

47. Roger AJ, Svärd SG, Tovar J, Clark CG, Smith MW, et al. A mitochondrial-like chaperonin 60 gene in Giardia lamblia: Evidence that diplomonads once harbored an endosymbiont related to the progenitor of mitochondria. Proc Nat Acad Sci USA 1998; 95: 229-234. doi:10.1073/pnas.95.1.229.

48. Marienfeld J, Unseld M, Brennicke A. The mitochondrial genome of Arabidopsis is composed of both native and immigrant information. Trends Plant Sci. 1999;4(12):495-502. doi:10.1016/s1360-1385(99)01502-2.

49. Hashimoto T, Sánchez LB, Shirakura T, Müller M, Hasegawa M. Secondary absence of mitochondria in Giardia lamblia and Trichomonas vaginalis revealed by valyl-tRNA synthetase phylogeny. Proc Natl Acad Sci U S A. 1998;95(12):6860-6865. doi:10.1073/pnas.95.12.6860.

50. Muller F, Brissac T, Le Bris N, Felbeck H, Gros O. First description of giant Archaea (Thaumarchaeota) associated with putative bacterial ectosymbionts in a sulfidic marine habitat. Environ Microbiol. 2010;12(8):2371-2383. doi:10.1111/j.1462-2920.2010.02309.x.

51. Yutin N, Wolf MY, Wolf YI, Koonin EV. The origins of phagocytosis and eukaryogenesis. Biol Direct. 2009;4:9. Published 2009 Feb 26. doi:10.1186/1745-6150-4-9.

52. Baum DA, Baum B. An inside-out origin for the eukaryotic cell. BMC Biol. 2014;12:76. Published 2014 Oct 28. doi:10.1186/s12915-014-0076-2.

53. Da Cunha V, Gaia M, Gadelle D, Nasir A, Forterre P. Lokiarchaea are close relatives of Euryarchaeota, not bridging the gap between prokaryotes and eukaryotes. PLoS Genet. 2017;13(6):e1006810. Published 2017 Jun 12. doi:10.1371/journal.pgen.1006810.

54. Forterre P. The origin of DNA genomes and DNA replication proteins. Curr Opin Microbiol. 2002;5(5):525-532. doi:10.1016/s1369-5274(02)00360-0

55. Reysenbach AL, Liu Y, Banta AB, et al. A ubiquitous thermoacidophilic archaeon from deep-sea hydrothermal vents. Nature. 2006;442(7101):444-447. doi:10.1038/nature04921.

56. Capella-Gutiérrez S, Marcet-Houben M, Gabaldón T. Phylogenomics supports microsporidia as the earliest diverging clade of sequenced fungi. BMC Biol. 2012;10:47. Published 2012 May 31. doi:10.1186/1741-7007-10-47.

57. James TY, Kauff F, Schoch CL, et al. Reconstructing the early evolution of Fungi using a six-gene phylogeny. Nature. 2006;443(7113):818-822. doi:10.1038/nature05110.

58. Corradi N, Keeling PJ. Microsporidia: a journey through radical taxonomical revisions. Fungal Biol Rev. Published online 2009. doi:10.1016/j.fbr.2009.05.001.

59. Cuomo CA, Desjardins CA, Bakowski MA, et al. Microsporidian genome analysis reveals evolutionary strategies for obligate intracellular growth. Genome Res. 2012;22(12):2478-2488. doi:10.1101/gr.142802.112.

60. Li T, Fang Z, He Q, Yu B, Zhou Z. Characterizing the xenoma of Varimorpha necatrix provides insights into the most efficient mode of Microsporidian proliferation. Front Cell Infect Microbiology 2021. Doi: 10.3389/fcimb.2021. 699239.

61. Nelson-Sathi S, Sousa FL, Roettger M, et al. Origins of major archaeal clades correspond to gene acquisitions from bacteria. Nature. 2015;517(7532):77-80. doi:10.1038/nature13805.

62. Woese CR, Kandler O, Wheelis ML. Towards a natural system of organisms: proposal for the domains Archaea, Bacteria, and Eucarya. Proc Natl Acad Sci U S A. 1990;87(12):4576-4579. doi:10.1073/pnas.87.12.4576.

63. Xue H, Tong KL, Marck C, Grosjean H, Wong JTF. Transfer RNA paralogs: evidence for genetic code-amino acid biosynthesis coevolution and an archaeal root of life. Gene. 2003;310:59-66. doi:10.1016/s0378-1119(03)00552-3.

64. Weiss MC, Preiner M, Xavier JC, Zimorski V, Martin WF. The last universal common ancestor between ancient Earth chemistry and the onset of genetics. PLoS Genet. Published online 2018. doi:10.1371/journal.pgen.1007518.

65. Blank CE. Low rates of lateral gene transfer among metabolic genes define the evolving biogeochemical niches of archaea through deep time. Archaea 2012; 2012: 23. Doi: 10.1155/2012/843539.

66. Wong JTF, Ng SK, Mat WK, Hu T, Xue H. Coevolution theory of the genetic code at age forty: pathway to translation and synthetic life. Life. 2016;6(1):12. Published 2016 Mar 16. doi:10.3390/life6010012.

67. Corliss JB, Dymond J, Gordon LI, et al. Submarine thermal springs on the Galápagos Rift. Science. Published online 1979. doi:10.1126/science.203.4385.1073

68. Baross JA, Hoffman SE. Submarine hydrothermal vents and associated gradient environments as sites for the origin and evolution of life. Orig Life Evol Biosph. Published online 1985. doi:10.1007/BF01808177

69. Wong TF, Chan CK, Xue H. Thermococcus-to-Clostridia pathway for the evolution of the Bacteria domain. bioRxiv. Preprint posted online January 11, 2023. https://doi.org/10.21203/rs.3.rs-2461311/v1

70. Nierhaus KH. Cited in Wong JTF, Root of Life. In Prebiotic Evolution and Astrobiology; Wong, JTF., Lazcano, A., eds.; Landes Bioscience: Austin, TX, USA, 2009; pp. 120–144. doi:10.1201/9781498713986.

71. Pech M, Karim Z, Yamamoto H, Kitakawa M, Qin Y, Nierhaus KH. Elongation factor 4 (EF4/LepA) accelerates protein synthesis at increased Mg2+ concentrations. Proc Natl Acad Sci U S A. 2011;108(8):3199-3203. doi:10.1073/pnas.1012994108