Primary endosymbiosis: have cyanobacteria and Chlamydiae ever been roommates? (original) (raw)

Mereschkowsky C. Über Natur und Ursprung der Chromatophoren im Pflanzenreiche. Biol Cent. 1905;25(18):593–604.

Margulis L. Symbiosis and evolution. Sci Am. 1971;225(2):48–57.

Martin W, Kowallik K. Annotated English translation of Mereschkowsky’s 1905 paper “Über Natur und Ursprung der Chromatophoren imPflanzenreiche.” Eur J Phycol. 1999;34(3):287–295. http://dx.doi.org/10.1080/09670269910001736342

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

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

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

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

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

Gutensohn M, Fan E, Frielingsdorf S, Hanner P, Hou B, Hust B, et al. Toc, Tic, Tat et al.: structure and function of protein transport machineries in chloroplasts. J Plant Physiol. 2006;163(3):333–347. http://dx.doi.org/10.1016/j.jplph.2005.11.009

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

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

Chan KX, Crisp PA, Estavillo GM, Pogson BJ. Chloroplast-to-nucleus communication: current knowledge, experimental strategies and relationship to drought stress signaling. Plant Signal Behav. 2010;5(12):1575–1582. http://dx.doi.org/10.4161/psb.5.12.13758

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

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

Yoon HS, Nakayama T, Reyes-Prieto A, Andersen RA, Boo SM, Ishida K, et al. A single origin of the photosynthetic organelle in different Paulinella lineages. BMC Evol Biol. 2009;9(1):98. http://dx.doi.org/10.1186/1471-2148-9-98

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

Mackiewicz P, Bodył A, Gagat P. Possible import routes of proteins into the cyanobacterial endosymbionts/plastids of Paulinella chromatophora. Theory Biosci. 2012;131(1):1–18. http://dx.doi.org/10.1007/s12064-011-0147-7

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

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

Ribeiro S, Golding GB. The mosaic nature of the eukaryotic nucleus. Mol Biol Evol. 1998;15(7):779–788.

Anantharaman V, Koonin EV, Aravind L. Comparative genomics and evolution of proteins involved in RNA metabolism. Nucl Acids Res. 2002;30(7):1427–1464.

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.

Esser C. A genome phylogeny for mitochondria among alpha-proteobacteria and a predominantly eubacterial ancestry of yeast nuclear genes. Mol Biol Evol. 2004;21(9):1643–1660. http://dx.doi.org/10.1093/molbev/msh160

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

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

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

Thiergart T, Landan G, Schenk M, Dagan T, Martin WF. An evolutionary network of genes present in the eukaryote common ancestor polls genomes on eukaryotic and mitochondrial origin. Genome Biol Evol. 2012;4(4):466–485. http://dx.doi.org/10.1093/gbe/evs018

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

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 cyanobacterial genes in the nucleus. Proc Natl Acad Sci USA. 2002;99(19):12246–12251. http://dx.doi.org/10.1073/pnas.182432999

Reyes-Prieto A, Hackett JD, Soares MB, Bonaldo MF, Bhattacharya D. Cyanobacterial contribution to algal nuclear genomes is primarily limited to plastid functions. Curr Biol. 2006;16(23):2320–2325. http://dx.doi.org/10.1016/j.cub.2006.09.063

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

Dagan T, Roettger M, Stucken K, Landan G, Koch R, Major P, et al. Genomes of Stigonematalean cyanobacteria (subsection V) and the evolution of oxygenic photosynthesis from prokaryotes to plastids. Genome Biol Evol. 2013;5(1):31–44. http://dx.doi.org/10.1093/gbe/evs117

Reyes-Prieto A, Moustafa A. Plastid-localized amino acid biosynthetic pathways of Plantae are predominantly composed of non-cyanobacterial enzymes. Sci Rep. 2012;2:955. http://dx.doi.org/10.1038/srep00955

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

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

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

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

Kamneva OK, Knight SJ, Liberles DA, Ward NL. Analysis of genome content evolution in pvc bacterial super-phylum: assessment of candidate genes associated with cellular organization and lifestyle. Genome Biol Evol. 2012;4(12):1375–1390. http://dx.doi.org/10.1093/gbe/evs113

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

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

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

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

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

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

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

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

Moustafa A, Reyes-Prieto A, Bhattacharya D. Chlamydiae has contributed at least 55 genes to Plantae with predominantly plastid functions. PLoS ONE. 2008;3(5):e2205. http://dx.doi.org/10.1371/journal.pone.0002205

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

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

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

Ball SG, Subtil A, Bhattacharya D, Moustafa A, Weber APM, Gehre L, et al. Metabolic effectors secreted by bacterial pathogens: essential facilitators of plastid endosymbiosis? Plant Cell. 2013;25(1):7–21. http://dx.doi.org/10.1105/tpc.112.101329

Reinhold T, Alawady A, Grimm B, Beran KC, Jahns P, Conrath U, et al. Limitation of nocturnal import of ATP into Arabidopsis chloroplasts leads to photooxidative damage. Plant J. 2007;50(2):293–304. http://dx.doi.org/10.1111/j.1365-313X.2007.03049.x

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

Deschamps P, Colleoni C, Nakamura Y, Suzuki E, Putaux JL, Buléon A, et al. Metabolic symbiosis and the birth of the plant kingdom. Mol Biol Evol. 2008;25(3):536–548. http://dx.doi.org/10.1093/molbev/msm280

Nakamura Y, Takahashi J, Sakurai A, Inaba Y, Suzuki E, Nihei S, et al. Some cyanobacteria synthesize semi-amylopectin type alpha-polyglucans instead of glycogen. Plant Cell Physiol. 2005;46(3):539–545. http://dx.doi.org/10.1093/pcp/pci045

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

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).

Deschamps P, Moreau H, Worden AZ, Dauvillée D, Ball SG. Early gene duplication within chloroplastida and its correspondence with relocation of starch metabolism to chloroplasts. Genetics. 2008;178(4):2373–2387. http://dx.doi.org/10.1534/genetics.108.087205

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

Colleoni C, Linka M, Deschamps P, Handford MG, Dupree P, Weber APM, et al. Phylogenetic and biochemical evidence supports the recruitment of an ADP-glucose translocator for the export of photosynthate during plastid endosymbiosis. Mol Biol Evol. 2010;27(12):2691–2701. http://dx.doi.org/10.1093/molbev/msq158

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

Facchinelli F, Pribil M, Oster U, Ebert NJ, Bhattacharya D, Leister D, et al. Proteomic analysis of the Cyanophora paradoxa muroplast provides clues on early events in plastid endosymbiosis. Planta. 2013;237(2):637–651. http://dx.doi.org/10.1007/s00425-012-1819-3

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.

Price DC, Chan CX, Yoon HS, Yang EC, Qiu H, Weber APM, et al. Cyanophora paradoxa genome elucidates origin of photosynthesis in algae and plants. Science. 2012;335(6070):843–847. http://dx.doi.org/10.1126/science.1213561

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

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

Keeling PJ, Burki F, Wilcox HM, Allam B, Allen EE, Amaral-Zettler LA, et al. The marine microbial eukaryote transcriptome sequencing project (MMETSP): illuminating the functional diversity of eukaryotic life in the oceans through transcriptome sequencing. PLoS Biol. 2014;12(6):e1001889. http://dx.doi.org/10.1371/journal.pbio.1001889

Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, et al. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucl Acids Res. 1997;25(17):3389–3402. http://dx.doi.org/10.1093/nar/25.17.3389

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

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

Criscuolo A, Gribaldo S. BMGE (block mapping and gathering with entropy): a new software for selection of phylogenetic informative regions from multiple sequence alignments. BMC Evol Biol. 2010;10(1):210. http://dx.doi.org/10.1186/1471-2148-10-210

Price MN, Dehal PS, Arkin AP. FastTree 2 – approximately maximum-likelihood trees for large alignments. PLoS ONE. 2010;5(3):e9490. http://dx.doi.org/10.1371/journal.pone.0009490

Jobb G, von Haeseler A, Strimmer K. TREEFINDER: a powerful graphical analysis environment for molecular phylogenetics. BMC Evol Biol. 2004;4(1):18. http://dx.doi.org/10.1186/1471-2148-4-18

Lamesch P, Berardini TZ, Li D, Swarbreck D, Wilks C, Sasidharan R, et al. The Arabidopsis information resource (TAIR): improved gene annotation and new tools. Nucl Acids Res. 2012;40(D1):D1202–D1210. http://dx.doi.org/10.1093/nar/gkr1090

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

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

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