PL EN


Preferencje help
Widoczny [Schowaj] Abstrakt
Liczba wyników
2014 | 83 | 4 |
Tytuł artykułu

Primary endosymbiosis: have cyanobacteria and Chlamydiae ever been roommates?

Autorzy
Treść / Zawartość
Warianty tytułu
Języki publikacji
EN
Abstrakty
EN
Eukaryotes acquired the ability to process photosynthesis by engulfing a cyanobacterium and transforming it into a genuine organelle called the plastid. This event, named primary endosymbiosis, occurred once more than a billion years ago, and allowed the emergence of the Archaeplastida, a monophyletic supergroup comprising the green algae and plants, the red algae and the glaucophytes. Of the other known cases of symbiosis between cyanobacteria and eukaryotes, none has achieved a comparable level of cell integration nor reached the same evolutionary and ecological success than primary endosymbiosis did. Reasons for this unique accomplishment are still unknown and difficult to comprehend. The exploration of plant genomes has revealed a considerable amount of genes closely related to homologs of Chlamydiae bacteria, and probably acquired by horizontal gene transfer. Several studies have proposed that these transferred genes, which are mostly involved in the functioning of the plastid, may have helped the settlement of primary endosymbiosis. Some of these studies propose that Chlamydiae and cyanobacterial symbionts coexisted in the eukaryotic host of the primary endosymbiosis, and that Chlamydiae provided solutions for the metabolic symbiosis between the cyanobacterium and the host, ensuring the success of primary endosymbiosis. In this review, I present a reevaluation of the contribution of Chlamydiae genes to the genome of Archaeplastida and discuss the strengths and weaknesses of this tripartite model for primary endosymbiosis.
Wydawca
-
Rocznik
Tom
83
Numer
4
Opis fizyczny
p.291-302,fig.,ref.
Twórcy
autor
  • Unite d’Ecologie, Systematique et Evolution, CNRS UMR 8079, Universite Paris-Sud, 91405 Orsay, France
Bibliografia
  • 1. Mereschkowsky C. Über Natur und Ursprung der Chromatophoren im Pflanzenreiche. Biol Cent. 1905;25(18):593–604.
  • 2. Margulis L. Symbiosis and evolution. Sci Am. 1971;225(2):48–57.
  • 3. Martin W, Kowallik K. Annotated English translation of Mereschkowsky’s 1905 paper “Über Natur und Ursprung der ChromatophorenimPflanzenreiche.” Eur J Phycol. 1999;34(3):287–295. http://dx.doi.org/10.1080/09670269910001736342
  • 4. Adl SM, Simpson AGB, Lane CE, Lukeš J, Bass D, Bowser SS, et al. The revised classification of eukaryotes. J Eukaryot Microbiol. 2012;59(5):429–514. http://dx.doi.org/10.1111/j.1550-7408.2012.00644.x
  • 5. Rodríguez-Ezpeleta N, Brinkmann H, Burey SC, Roure B, Burger G, Löffelhardt W, et al. Monophyly of primary photosynthetic eukaryotes:green plants, red algae, and glaucophytes. Curr Biol. 2005;15(14):1325–1330. http://dx.doi.org/10.1016/j.cub.2005.06.040
  • 6. Moreira D, Le Guyader H, Philippe H. The origin of red algae and the evolution of chloroplasts. Nature. 2000;405(6782):69–72. http://dx.doi.org/10.1038/35011054
  • 7. Martin W, Brinkmann H, Savonna C, Cerff R. Evidence for a chimeric nature of nuclear genomes: eubacterial origin of eukaryotic glyceraldehyde- 3-phosphate dehydrogenase genes. Proc Natl Acad Sci USA.1993;90(18):8692–8696. http://dx.doi.org/10.1073/pnas.90.18.8692
  • 8. Martin W, Stoebe B, Goremykin V, Hapsmann S, Hasegawa M, Kowallik KV. Gene transfer to the nucleus and the evolution of chloroplasts.Nature. 1998;393(6681):162–165. http://dx.doi.org/10.1038/30234
  • 9. Gutensohn M, Fan E, Frielingsdorf S, Hanner P, Hou B, Hust B, et al. Toc, Tic, Tat et al.: structure and function of protein transportmachineries in chloroplasts. J Plant Physiol. 2006;163(3):333–347.http://dx.doi.org/10.1016/j.jplph.2005.11.009
  • 10. Steiner JM, Löffelhardt W. Protein import into cyanelles. Trends Plant Sci. 2002;7(2):72–77. http://dx.doi.org/10.1016/ S1360-1385(01)02179-3
  • 11. Koussevitzky S, Nott A, Mockler TC, Hong F, Sachetto-Martins G, Surpin M, et al. Signals from chloroplasts converge to regulate nuclear gene expression. Science. 2007;316(5825):715–719. http://dx.doi.org/10.1126/science.1140516
  • 12. Chan KX, Crisp PA, Estavillo GM, Pogson BJ. Chloroplast-tonucleus communication: current knowledge, experimental strategiesand relationship to drought stress signaling. Plant Signal Behav.2010;5(12):1575–1582. http://dx.doi.org/10.4161/psb.5.12.13758
  • 13. Keeling PJ. The endosymbiotic origin, diversification and fate of plastids. Phil Trans R Soc Lond B. 2010;365(1541):729–748. http:// dx.doi.org/10.1098/rstb.2009.0103
  • 14. Marin B, M. Nowack EC, Melkonian M. A plastid in the making: evidence for a second primary endosymbiosis. Protist. 2005;156(4):425–432. http://dx.doi.org/10.1016/j.protis.2005.09.001
  • 15. Yoon HS, Nakayama T, Reyes-Prieto A, Andersen RA, Boo SM, Ishida K, et al. A single origin of the photosynthetic organelle in differentPaulinella lineages. BMC Evol Biol. 2009;9(1):98. http://dx.doi.org/10.1186/1471-2148-9-98
  • 16. Nowack ECM, Vogel H, Groth M, Grossman AR, Melkonian M, Glockner G. Endosymbiotic gene transfer and transcriptional regulation of transferred genes in Paulinella chromatophora. Mol Biol Evol. 2011;28(1):407–422. http://dx.doi.org/10.1093/molbev/msq209
  • 17. Mackiewicz P, Bodył A, Gagat P. Possible import routes of proteins into the cyanobacterial endosymbionts/plastids of Paulinellachromatophora. Theory Biosci. 2012;131(1):1–18. http://dx.doi.org/10.1007/s12064-011-0147-7
  • 18. Nowack ECM, Grossman AR. Trafficking of protein into the recently established photosynthetic organelles of Paulinella chromatophora.Proc Natl Acad Sci USA. 2012;109(14):5340–5345. http://dx.doi.org/10.1073/pnas.1118800109
  • 19. Simonson AB, Servin JA, Skophammer RG, Herbold CW, Rivera MC, Lake JA. Decoding the genomic tree of life. Proc Natl Acad Sci USA. 2005;102(1 suppl):6608–6613. http://dx.doi.org/10.1073/ pnas.0501996102
  • 20. Ribeiro S, Golding GB. The mosaic nature of the eukaryotic nucleus. Mol Biol Evol. 1998;15(7):779–788.
  • 21. Anantharaman V, Koonin EV, Aravind L. Comparative genomics and evolution of proteins involved in RNA metabolism. Nucl Acids Res.2002;30(7):1427–1464.
  • 22. Langer D, Hain J, Thuriaux P, Zillig W. Transcription in archaea: similarity to that in eucarya. Proc Natl Acad Sci USA.1995;92(13):5768–5772.
  • 23. Esser C. A genome phylogeny for mitochondria among alphaproteobacteria and a predominantly eubacterial ancestry of yeastnuclear genes. Mol Biol Evol. 2004;21(9):1643–1660. http://dx.doi.org/10.1093/molbev/msh160
  • 24. López-Garćia P, Moreira D. Metabolic symbiosis at the origin of eukaryotes. Trends Biochem Sci. 1999;24(3):88–93. http://dx.doi. org/10.1016/S0968-0004(98)01342-5
  • 25. Martin W, Müller M. The hydrogen hypothesis for the first eukaryote. Nature. 1998;392(6671):37–41. http://dx.doi.org/10.1038/32096
  • 26. Martin W. Archaebacteria (Archaea) and the origin of the eukaryotic nucleus. Curr Opin Microbiol. 2005;8(6):630–637. http://dx.doi.org/10.1016/j.mib.2005.10.004
  • 27. Thiergart T, Landan G, Schenk M, Dagan T, Martin WF. An evolutionary network of genes present in the eukaryote common ancestor pollsgenomes on eukaryotic and mitochondrial origin. Genome Biol Evol.2012;4(4):466–485. http://dx.doi.org/10.1093/gbe/evs018
  • 28. Rochette NC, Brochier-Armanet C, Gouy M. Phylogenomic test of the hypotheses for the evolutionary origin of eukaryotes. Mol Biol Evol. 2014;31(4):832–845. http://dx.doi.org/10.1093/molbev/mst272
  • 29. Martin W, Rujan T, Richly E, Hansen A, Cornelsen S, Lins T, et al. Evolutionary analysis of Arabidopsis, cyanobacterial, and chloroplast genomes reveals plastid phylogeny and thousands of cyanobacterialgenes in the nucleus. Proc Natl Acad Sci USA. 2002;99(19):12246–12251. http://dx.doi.org/10.1073/pnas.182432999
  • 30. Reyes-Prieto A, Hackett JD, Soares MB, Bonaldo MF, Bhattacharya D. Cyanobacterial contribution to algal nuclear genomes is primarilylimited to plastid functions. Curr Biol. 2006;16(23):2320–2325. http://dx.doi.org/10.1016/j.cub.2006.09.063
  • 31. Deusch O, Landan G, Roettger M, Gruenheit N, Kowallik KV, Allen JF, et al. Genes of cyanobacterial origin in plant nuclear genomes point to a heterocyst-forming plastid ancestor. Mol Biol Evol. 2008;25(4):748–761. http://dx.doi.org/10.1093/molbev/msn022
  • 32. Dagan T, Roettger M, Stucken K, Landan G, Koch R, Major P, et al. Genomes of Stigonematalean cyanobacteria (subsection V) and theevolution of oxygenic photosynthesis from prokaryotes to plastids.Genome Biol Evol. 2013;5(1):31–44. http://dx.doi.org/10.1093/gbe/evs117
  • 33. Reyes-Prieto A, Moustafa A. Plastid-localized amino acid biosynthetic pathways of Plantae are predominantly composed of non-cyanobacterialenzymes. Sci Rep. 2012;2:955. http://dx.doi.org/10.1038/srep00955
  • 34. Qiu H, Price DC, Weber APM, Facchinelli F, Yoon HS, Bhattacharya D. Assessing the bacterial contribution to the plastid proteome.Trends Plant Sci. 2013;18(12):680–687. http://dx.doi.org/10.1016/j.tplants.2013.09.007
  • 35. Suzuki K, Miyagishima SY. Eukaryotic and eubacterial contributions to the establishment of plastid proteome estimated by large-scale phylogenetic analyses. Mol Biol Evol. 2010;27(3):581–590. http://dx.doi.org/10.1093/molbev/msp273
  • 36. Stegemann S, Bock R. Experimental reconstruction of functional gene transfer from the tobacco plastid genome to the nucleus. Plant Cell.2006;18(11):2869–2878. http://dx.doi.org/10.1105/tpc.106.046466
  • 37. Zimorski V, Ku C, Martin WF, Gould SB. Endosymbiotic theory for organelle origins. Curr Opin Microbiol. 2014;22:38–48. http://dx.doi.org/10.1016/j.mib.2014.09.008
  • 38. Kamneva OK, Knight SJ, Liberles DA, Ward NL. Analysis of genome content evolution in pvc bacterial super-phylum: assessment of candidategenes associated with cellular organization and lifestyle. GenomeBiol Evol. 2012;4(12):1375–1390. http://dx.doi.org/10.1093/gbe/evs113
  • 39. Horn M, Collingro A, Schmitz-Esser S, Beier CL, Purkhold U, Fartmann B, et al. Illuminating the evolutionary history of chlamydiae. Science. 2004;304(5671):728–730. http://dx.doi. org/10.1126/science.1096330
  • 40. Horn M. Chlamydiae as symbionts in eukaryotes. Annu Rev Microbiol. 2008;62(1):113–131. http://dx.doi.org/10.1146/annurev.micro.62.081307.162818
  • 41. Wolf YI, Aravind L, Koonin EV. Rickettsiae and Chlamydiae: evidence of horizontal gene transfer and gene exchange. Trends Genet.1999;15(5):173–175. http://dx.doi.org/10.1016/S0168-9525(99)01704-7
  • 42. Haferkamp I, Schmitz-Esser S, Wagner M, Neigel N, Horn M, Neuhaus HE. Tapping the nucleotide pool of the host:novel nucleotide carrier proteins of Protochlamydia amoebophila.Mol Microbiol. 2006;60(6):1534–1545. http://dx.doi.org/10.1111/j.1365-2958.2006.05193.x
  • 43. Schwöppe C, Winkler HH, Neuhaus HE. Properties of the glucose-6-phosphate transporter from Chlamydia pneumoniae (HPTcp)and the glucose-6-phosphate sensor from Escherichia coli (UhpC).J Bacteriol. 2002;184(8):2108–2115. http://dx.doi.org/10.1128/JB.184.8.2108-2115.2002
  • 44. Subtil A, Collingro A, Horn M. Tracing the primordial Chlamydiae: extinct parasites of plants? Trends Plant Sci. 2014;19(1):36–43. http://dx.doi.org/10.1016/j.tplants.2013.10.005
  • 45. Becker B, Hoef-Emden K, Melkonian M. Chlamydial genes shed light on the evolution of photoautotrophic eukaryotes. BMC Evol Biol.2008;8(1):203. http://dx.doi.org/10.1186/1471-2148-8-203
  • 46. Huang J, Gogarten J. Did an ancient chlamydial endosymbiosis facilitate the establishment of primary plastids? Genome Biol.2007;8(6):R99. http://dx.doi.org/10.1186/gb-2007-8-6-r99
  • 47. Moustafa A, Reyes-Prieto A, Bhattacharya D. Chlamydiae has contributed at least 55 genes to Plantae with predominantly plastidfunctions. PLoS ONE. 2008;3(5):e2205. http://dx.doi.org/10.1371/journal.pone.0002205
  • 48. Brinkman FSL, Blanchard JL, Cherkasov A, Av-Gay Y, Brunham RC, Fernandez RC, et al. Evidence that plant-like genes in Chlamydia species reflect an ancestral relationship between Chlamydiaceae, cyanobacteria,and the chloroplast. Genome Res. 2002;12(8):1159–1167. http://dx.doi.org/10.1101/gr.341802
  • 49. Stephens RS. Genome sequence of an obligate intracellular pathogen of humans: Chlamydia trachomatis. Science. 1998;282(5389):754–759.http://dx.doi.org/10.1126/science.282.5389.754
  • 50. Collingro A, Tischler P, Weinmaier T, Penz T, Heinz E, Brunham RC, et al. Unity in variety – the pan-genome of the Chlamydiae. Mol Biol Evol.2011;28(12):3253–3270. http://dx.doi.org/10.1093/molbev/msr161
  • 51. Ball SG, Subtil A, Bhattacharya D, Moustafa A, Weber APM, Gehre L, et al. Metabolic effectors secreted by bacterial pathogens: essentialfacilitators of plastid endosymbiosis? Plant Cell. 2013;25(1):7–21.http://dx.doi.org/10.1105/tpc.112.101329
  • 52. Reinhold T, Alawady A, Grimm B, Beran KC, Jahns P, Conrath U, et al. Limitation of nocturnal import of ATP into Arabidopsis chloroplastsleads to photooxidative damage. Plant J. 2007;50(2):293–304. http://dx.doi.org/10.1111/j.1365-313X.2007.03049.x
  • 53. Watkins RF, Gray MW. The frequency of eubacterium-to-eukaryote lateral gene transfers shows significant cross-taxa variation within amoebozoa. J Mol Evol. 2006;63(6):801–814. http://dx.doi.org/10.1007/ s00239-006-0031-0
  • 54. Deschamps P, Colleoni C, Nakamura Y, Suzuki E, Putaux JL, Buléon A, et al. Metabolic symbiosis and the birth of the plant kingdom. Mol BiolEvol. 2008;25(3):536–548. http://dx.doi.org/10.1093/molbev/msm280
  • 55. Nakamura Y, Takahashi J, Sakurai A, Inaba Y, Suzuki E, Nihei S, et al. Some cyanobacteria synthesize semi-amylopectin type alpha-polyglucansinstead of glycogen. Plant Cell Physiol. 2005;46(3):539–545.http://dx.doi.org/10.1093/pcp/pci045
  • 56. Gallon JR. The oxygen sensitivity of nitrogenase: a problem for biochemists and micro-organisms. Trends Biochem Sci. 1981;6:19–23.http://dx.doi.org/10.1016/0968-0004(81)90008-6
  • 57. Wolk CP, Ernst A, Elhai J. Heterocyst metabolism and development. In: Bryant DA, editor. The molecular biology of cyanobacteria. Dordrecht: Springer; 2004. p. 769–823. (Advances in photosynthesis and respiration; vol 1).
  • 58. Deschamps P, Moreau H, Worden AZ, Dauvillée D, Ball SG. Early gene duplication within chloroplastida and its correspondencewith relocation of starch metabolism to chloroplasts. Genetics.2008;178(4):2373–2387. http://dx.doi.org/10.1534/genetics.108.087205
  • 59. Deschamps P, Haferkamp I, d’ Hulst C, Neuhaus HE, Ball SG. The relocation of starch metabolism to chloroplasts: when, why and how. Trends Plant Sci. 2008;13(11):574–582. http://dx.doi.org/10.1016/j.tplants.2008.08.009
  • 60. Colleoni C, Linka M, Deschamps P, Handford MG, Dupree P, Weber APM, et al. Phylogenetic and biochemical evidence supports therecruitment of an ADP-glucose translocator for the export of photosynthateduring plastid endosymbiosis. Mol Biol Evol. 2010;27(12):2691–2701. http://dx.doi.org/10.1093/molbev/msq158
  • 61. Lu C, Lei L, Peng B, Tang L, Ding H, Gong S, et al. Chlamydia trachomatis GlgA is secreted into host cell cytoplasm. PLoS ONE.2013;8(7):e68764. http://dx.doi.org/10.1371/journal.pone.0068764
  • 62. Facchinelli F, Pribil M, Oster U, Ebert NJ, Bhattacharya D, Leister D, et al. Proteomic analysis of the Cyanophora paradoxa muroplastprovides clues on early events in plastid endosymbiosis. Planta.2013;237(2):637–651. http://dx.doi.org/10.1007/s00425-012-1819-3
  • 63. Shattuck-Eidens DM, Kadner RJ. Molecular cloning of the uhp region and evidence for a positive activator for expression of the hexose phosphate transport system of Escherichia coli. J Bacteriol.1983;155(3):1062–1070.
  • 64. Price DC, Chan CX, Yoon HS, Yang EC, Qiu H, Weber APM, et al. Cyanophora paradoxa genome elucidates origin of photosynthesisin algae and plants. Science. 2012;335(6070):843–847. http://dx.doi.org/10.1126/science.1213561
  • 65. Rockwell NC, Lagarias JC, Bhattacharya D. Primary endosymbiosis and the evolution of light and oxygen sensing in photosynthetic eukaryotes. Front Ecol Evol. 2014;2:66. http://dx.doi.org/10.3389/ fevo.2014.00066
  • 66. Facchinelli F, Colleoni C, Ball SG, Weber APM. Chlamydia, cyanobiont, or host: who was on top in the ménage à trois? Trends Plant Sci.2013;18(12):673–679. http://dx.doi.org/10.1016/j.tplants.2013.09.006
  • 67. Keeling PJ, Burki F, Wilcox HM, Allam B, Allen EE, Amaral-Zettler LA, et al. The marine microbial eukaryote transcriptome sequencingproject (MMETSP): illuminating the functional diversity of eukaryoticlife in the oceans through transcriptome sequencing. PLoS Biol.2014;12(6):e1001889. http://dx.doi.org/10.1371/journal.pbio.1001889
  • 68. Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, et al. Gapped BLAST and PSI-BLAST: a new generation of proteindatabase search programs. Nucl Acids Res. 1997;25(17):3389–3402.http://dx.doi.org/10.1093/nar/25.17.3389
  • 69. Pruitt KD, Tatusova T, Maglott DR. NCBI reference sequences (RefSeq): a curated non-redundant sequence database of genomes, transcripts and proteins. Nucl Acids Res. 2007;35(database):D61–D65. http://dx.doi.org/10.1093/nar/gkl842
  • 70. Katoh K, Toh H. Recent developments in the MAFFT multiple sequence alignment program. Brief Bioinform. 2008;9(4):286–298.http://dx.doi.org/10.1093/bib/bbn013
  • 71. Criscuolo A, Gribaldo S. BMGE (block mapping and gathering with entropy): a new software for selection of phylogenetic informativeregions from multiple sequence alignments. BMC Evol Biol. 2010;10(1):210. http://dx.doi.org/10.1186/1471-2148-10-210
  • 72. Price MN, Dehal PS, Arkin AP. FastTree 2 – approximately maximumlikelihood trees for large alignments. PLoS ONE. 2010;5(3):e9490.http://dx.doi.org/10.1371/journal.pone.0009490
  • 73. Jobb G, von Haeseler A, Strimmer K. TREEFINDER: a powerful graphical analysis environment for molecular phylogenetics. BMCEvol Biol. 2004;4(1):18. http://dx.doi.org/10.1186/1471-2148-4-18
  • 74. Lamesch P, Berardini TZ, Li D, Swarbreck D, Wilks C, Sasidharan R, et al. The Arabidopsis information resource (TAIR): improved geneannotation and new tools. Nucl Acids Res. 2012;40(D1):D1202–D1210.http://dx.doi.org/10.1093/nar/gkr1090
  • 75. Keeling PJ, Palmer JD. Horizontal gene transfer in eukaryotic evolution. Nat Rev Genet. 2008;9(8):605–618. http://dx.doi.org/10.1038/nrg2386
  • 76. Marcet-Houben M, Gabaldón T. Acquisition of prokaryotic genes by fungal genomes. Trends Genet. 2010;26(1):5–8. http://dx.doi.org/10.1016/j.tig.2009.11.007
  • 77. Henrissat B, Deleury E, Coutinho PM. Glycogen metabolism loss: a common marker of parasitic behaviour in bacteria? Trends Genet.2002;18(9):437–440. http://dx.doi.org/10.1016/S0168-9525(02)02734-8
Typ dokumentu
Bibliografia
Identyfikatory
Identyfikator YADDA
bwmeta1.element.agro-2f6af265-9dd0-47cc-a869-8c4ecca58c61
JavaScript jest wyłączony w Twojej przeglądarce internetowej. Włącz go, a następnie odśwież stronę, aby móc w pełni z niej korzystać.