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Philos Trans R Soc Lond B Biol Sci. 2003 January 29; 358(1429): 5–518.
PMCID: PMC1693093

Genomes at the interface between bacteria and organelles.


The topic of the transition of the genome of a free-living bacterial organism to that of an organelle is addressed by considering three cases. Two of these are relatively clear-cut as involving respectively organisms (cyanobacteria) and organelles (plastids). Cyanobacteria are usually free-living but some are involved in symbioses with a range of eukaryotes in which the cyanobacterial partner contributes photosynthesis, nitrogen fixation, or both of these. In several of these symbioses the cyanobacterium is vertically transmitted, and in a few instances, sufficient unsuccessful attempts have been made to culture the cyanobiont independently for the association to be considered obligate for the cyanobacterium. Plastids clearly had a cyanobacterial ancestor but cannot grow independently of the host eukaryote. Plastid genomes have at most 15% of the number of genes encoded by the cyanobacterium with the smallest number of genes; more genes than are retained in the plastid genome have been transferred to the eukaryote nuclear genome, while the rest of the cyanobacterial genes have been lost. Even the most cyanobacteria-like plastids, for example the "cyanelles" of glaucocystophyte algae, are functionally and genetically very similar to other plastids and give little help in indicating intermediates in the evolution of plastids. The third case considered is the vertically transmitted intracellular bacterial symbionts of insects where the symbiosis is usually obligate for both partners. The number of genes encoded by the genomes of these obligate symbionts is intermediate between that of organelles and that of free-living bacteria, and the genomes of the insect symbionts also show rapid rates of sequence evolution and AT (adenine, thymine) bias. Genetically and functionally, these insect symbionts show considerable similarity to organelles.

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  • Akhmanova A, Voncken F, van Alen T, van Hoek A, Boxma B, Vogels G, Veenhuis M, Hackstein JH. A hydrogenosome with a genome. Nature. 1998 Dec 10;396(6711):527–528. [PubMed]
  • Akman L, Aksoy S. A novel application of gene arrays: Escherichia coli array provides insight into the biology of the obligate endosymbiont of tsetse flies. Proc Natl Acad Sci U S A. 2001 Jun 19;98(13):7546–7551. [PubMed]
  • Akman L, Rio RV, Beard CB, Aksoy S. Genome size determination and coding capacity of Sodalis glossinidius, an enteric symbiont of tsetse flies, as revealed by hybridization to Escherichia coli gene arrays. J Bacteriol. 2001 Aug;183(15):4517–4525. [PMC free article] [PubMed]
  • Allen JF. Control of gene expression by redox potential and the requirement for chloroplast and mitochondrial genomes. J Theor Biol. 1993 Dec 21;165(4):609–631. [PubMed]
  • Allen JF. Redox control of transcription: sensors, response regulators, activators and repressors. FEBS Lett. 1993 Oct 18;332(3):203–207. [PubMed]
  • Allen JF. Separate sexes and the mitochondrial theory of ageing. J Theor Biol. 1996 May 21;180(2):135–140. [PubMed]
  • Allen JF, Raven JA. Free-radical-induced mutation vs redox regulation: costs and benefits of genes in organelles. J Mol Evol. 1996 May;42(5):482–492. [PubMed]
  • Andersson SG, Kurland CG. Reductive evolution of resident genomes. Trends Microbiol. 1998 Jul;6(7):263–268. [PubMed]
  • Barbrook AC, Symington H, Nisbet RE, Larkum A, Howe CJ. Organisation and expression of the plastid genome of the dinoflagellate Amphidinium operculatum. Mol Genet Genomics. 2001 Dec;266(4):632–638. [PubMed]
  • Baumann P, Baumann L, Lai CY, Rouhbakhsh D, Moran NA, Clark MA. Genetics, physiology, and evolutionary relationships of the genus Buchnera: intracellular symbionts of aphids. Annu Rev Microbiol. 1995;49:55–94. [PubMed]
  • Beech PL, Gilson PR. FtsZ and organelle division in Protists. Protist. 2000 May;151(1):11–16. [PubMed]
  • Bergthorsson U, Ochman H. Distribution of chromosome length variation in natural isolates of Escherichia coli. Mol Biol Evol. 1998 Jan;15(1):6–16. [PubMed]
  • Berridge MJ, Bootman MD, Lipp P. Calcium--a life and death signal. Nature. 1998 Oct 15;395(6703):645–648. [PubMed]
  • Bhattacharya D, Helmchen T, Bibeau C, Melkonian M. Comparisons of nuclear-encoded small-subunit ribosomal RNAs reveal the evolutionary position of the Glaucocystophyta. Mol Biol Evol. 1995 May;12(3):415–420. [PubMed]
  • Blanchard JL, Lynch M. Organellar genes: why do they end up in the nucleus? Trends Genet. 2000 Jul;16(7):315–320. [PubMed]
  • Blattner FR, Plunkett G, 3rd, Bloch CA, Perna NT, Burland V, Riley M, Collado-Vides J, Glasner JD, Rode CK, Mayhew GF, et al. The complete genome sequence of Escherichia coli K-12. Science. 1997 Sep 5;277(5331):1453–1462. [PubMed]
  • Cheng Q, Aksoy S. Tissue tropism, transmission and expression of foreign genes in vivo in midgut symbionts of tsetse flies. Insect Mol Biol. 1999 Feb;8(1):125–132. [PubMed]
  • Chen X, Li S, Aksoy S. Concordant evolution of a symbiont with its host insect species: molecular phylogeny of genus Glossina and its bacteriome-associated endosymbiont, Wigglesworthia glossinidia. J Mol Evol. 1999 Jan;48(1):49–58. [PubMed]
  • Clark MA, Moran NA, Baumann P. Sequence evolution in bacterial endosymbionts having extreme base compositions. Mol Biol Evol. 1999 Nov;16(11):1586–1598. [PubMed]
  • Claus H, Martin HH, Jantos CA, König H. A search for beta-lactamase in chlamydiae, mycoplasmas, planctomycetes, and cyanelles: bacteria and bacterial descendants at different phylogenetic positions and stages of cell wall development. Microbiol Res. 2000 Apr;155(1):1–6. [PubMed]
  • Darby AC, Birkle LM, Turner SL, Douglas AE. An aphid-borne bacterium allied to the secondary symbionts of whitefly. FEMS Microbiol Ecol. 2001 Jun;36(1):43–50. [PubMed]
  • Douglas AE. Mycetocyte symbiosis in insects. Biol Rev Camb Philos Soc. 1989 Nov;64(4):409–434. [PubMed]
  • Douglas AE. Nutritional interactions in insect-microbial symbioses: aphids and their symbiotic bacteria Buchnera. Annu Rev Entomol. 1998;43:17–37. [PubMed]
  • Douglas SE, Penny SL. The plastid genome of the cryptophyte alga, Guillardia theta: complete sequence and conserved synteny groups confirm its common ancestry with red algae. J Mol Evol. 1999 Feb;48(2):236–244. [PubMed]
  • Ferriere Régis, Bronstein Judith L, Rinaldi Sergio, Law Richard, Gauduchon Mathias. Cheating and the evolutionary stability of mutualisms. Proc Biol Sci. 2002 Apr 22;269(1493):773–780. [PMC free article] [PubMed]
  • Galván Aurora, Rexach Jesús, Mariscal Vicente, Fernández Emilio. Nitrite transport to the chloroplast in Chlamydomonas reinhardtii: molecular evidence for a regulated process. J Exp Bot. 2002 Apr;53(370):845–853. [PubMed]
  • Gil Rosario, Sabater-Muñoz Beatriz, Latorre Amparo, Silva Francisco J, Moya Andrés. Extreme genome reduction in Buchnera spp.: toward the minimal genome needed for symbiotic life. Proc Natl Acad Sci U S A. 2002 Apr 2;99(7):4454–4458. [PubMed]
  • Glöckner G, Rosenthal A, Valentin K. The structure and gene repertoire of an ancient red algal plastid genome. J Mol Evol. 2000 Oct;51(4):382–390. [PubMed]
  • Görtz HD. Infections of Paramecium bursaria with bacteria and yeasts. J Cell Sci. 1982 Dec;58:445–453. [PubMed]
  • Green BJ, Li WY, Manhart JR, Fox TC, Summer EJ, Kennedy RA, Pierce SK, Rumpho ME. Mollusc-algal chloroplast endosymbiosis. Photosynthesis, thylakoid protein maintenance, and chloroplast gene expression continue for many months in the absence of the algal nucleus. Plant Physiol. 2000 Sep;124(1):331–342. [PubMed]
  • Hackstein JH, Akhmanova A, Voncken F, van Hoek A, van Alen T, Boxma B, Moon-van der Staay SY, van der Staay G, Leunissen J, Huynen M, et al. Hydrogenosomes: convergent adaptations of mitochondria to anaerobic environments. Zoology (Jena) 2001;104(3-4):290–302. [PubMed]
  • Hanten JJ, Pierce SK. Synthesis of several light-harvesting complex I polypeptides is blocked by cycloheximide in symbiotic chloroplasts in the sea slug, Elysia chlorotica (Gould): a case for horizontal gene transfer between alga and animal? Biol Bull. 2001 Aug;201(1):34–44. [PubMed]
  • Helmchen TA, Bhattacharya D, Melkonian M. Analyses of ribosomal RNA sequences from glaucocystophyte cyanelles provide new insights into the evolutionary relationships of plastids. J Mol Evol. 1995 Aug;41(2):203–210. [PubMed]
  • Henze K, Martin W. How do mitochondrial genes get into the nucleus? Trends Genet. 2001 Jul;17(7):383–387. [PubMed]
  • Hess WR, Rocap G, Ting CS, Larimer F, Stilwagen S, Lamerdin J, Chisholm SW. The photosynthetic apparatus of Prochlorococcus: Insights through comparative genomics. Photosynth Res. 2001;70(1):53–71. [PubMed]
  • Hoffman PF, Kaufman AJ, Halverson GP, Schrag DP. A neoproterozoic snowball earth . Science. 1998 Aug 28;281(5381):1342–1346. [PubMed]
  • Hongoh Y, Ishikawa H. Evolutionary studies on uricases of fungal endosymbionts of aphids and planthoppers. J Mol Evol. 2000 Sep;51(3):265–277. [PubMed]
  • Howe CJ, Barbrook AC, Lockhart PJ. Organelle genes--do they jump or are they pushed? Trends Genet. 2000 Feb;16(2):65–66. [PubMed]
  • JAMES G. Community resources for health education, how well are they being utilized in the school program? Am J Public Health Nations Health. 1948 Sep;38(9):1258–1262. [PubMed]
  • Joza N, Susin SA, Daugas E, Stanford WL, Cho SK, Li CY, Sasaki T, Elia AJ, Cheng HY, Ravagnan L, et al. Essential role of the mitochondrial apoptosis-inducing factor in programmed cell death. Nature. 2001 Mar 29;410(6828):549–554. [PubMed]
  • Kanevski I, Maliga P. Relocation of the plastid rbcL gene to the nucleus yields functional ribulose-1,5-bisphosphate carboxylase in tobacco chloroplasts. Proc Natl Acad Sci U S A. 1994 Mar 1;91(5):1969–1973. [PubMed]
  • Kirschvink JL, Gaidos EJ, Bertani LE, Beukes NJ, Gutzmer J, Maepa LN, Steinberger RE. Paleoproterozoic snowball earth: extreme climatic and geochemical global change and its biological consequences. Proc Natl Acad Sci U S A. 2000 Feb 15;97(4):1400–1405. [PubMed]
  • Lambert JD, Moran NA. Deleterious mutations destabilize ribosomal RNA in endosymbiotic bacteria. Proc Natl Acad Sci U S A. 1998 Apr 14;95(8):4458–4462. [PubMed]
  • Lawrence JG, Hendrix RW, Casjens S. Where are the pseudogenes in bacterial genomes? Trends Microbiol. 2001 Nov;9(11):535–540. [PubMed]
  • Lemieux C, Otis C, Turmel M. Ancestral chloroplast genome in Mesostigma viride reveals an early branch of green plant evolution. Nature. 2000 Feb 10;403(6770):649–652. [PubMed]
  • Lockhart PJ, Howe CJ, Bryant DA, Beanland TJ, Larkum AW. Substitutional bias confounds inference of cyanelle origins from sequence data. J Mol Evol. 1992 Feb;34(2):153–162. [PubMed]
  • McFadden GI. Endosymbiosis and evolution of the plant cell. Curr Opin Plant Biol. 1999 Dec;2(6):513–519. [PubMed]
  • McKay CP. Thickness of tropical ice and photosynthesis on a snowball Earth. Geophys Res Lett. 2000 Jul 15;27(14):2153–2156. [PubMed]
  • Mallick N, Rai LC, Mohn FH, Soeder CJ. Studies on nitric oxide (NO) formation by the green alga Scenedesmus obliquus and the diazotrophic cyanobacterium Anabaena doliolum. Chemosphere. 1999 Oct;39(10):1601–1610. [PubMed]
  • Mangeney E, Hawthornthwaite AM, Codd GA, Gibbs SP. Immunocytochemical Localization of Phosphoribulose Kinase in the Cyanelles of Cyanophora paradoxa and Glaucocystis nostochinearum. Plant Physiol. 1987 Aug;84(4):1028–1032. [PubMed]
  • Martin W, Stoebe B, Goremykin V, Hapsmann S, Hasegawa M, Kowallik KV. Gene transfer to the nucleus and the evolution of chloroplasts. Nature. 1998 May 14;393(6681):162–165. [PubMed]
  • Meeks JC, Elhai J, Thiel T, Potts M, Larimer F, Lamerdin J, Predki P, Atlas R. An overview of the genome of Nostoc punctiforme, a multicellular, symbiotic cyanobacterium. Photosynth Res. 2001;70(1):85–106. [PubMed]
  • Moran NA. Accelerated evolution and Muller's rachet in endosymbiotic bacteria. Proc Natl Acad Sci U S A. 1996 Apr 2;93(7):2873–2878. [PubMed]
  • Moran NA, Wernegreen JJ. Lifestyle evolution in symbiotic bacteria: insights from genomics. Trends Ecol Evol. 2000 Aug;15(8):321–326. [PubMed]
  • Moreira D, Le Guyader H, Philippe H. The origin of red algae and the evolution of chloroplasts. Nature. 2000 May 4;405(6782):69–72. [PubMed]
  • Morse D, Salois P, Markovic P, Hastings JW. A nuclear-encoded form II RuBisCO in dinoflagellates. Science. 1995 Jun 16;268(5217):1622–1624. [PubMed]
  • Morton BR. Selection on the codon bias of chloroplast and cyanelle genes in different plant and algal lineages. J Mol Evol. 1998 Apr;46(4):449–459. [PubMed]
  • Morton BR. Selection at the amino acid level can influence synonymous codon usage: implications for the study of codon adaptation in plastid genes. Genetics. 2001 Sep;159(1):347–358. [PubMed]
  • Pfanzagl B, Zenker A, Pittenauer E, Allmaier G, Martinez-Torrecuadrada J, Schmid ER, De Pedro MA, Löffelhardt W. Primary structure of cyanelle peptidoglycan of Cyanophora paradoxa: a prokaryotic cell wall as part of an organelle envelope. J Bacteriol. 1996 Jan;178(2):332–339. [PMC free article] [PubMed]
  • Race HL, Herrmann RG, Martin W. Why have organelles retained genomes? Trends Genet. 1999 Sep;15(9):364–370. [PubMed]
  • Rujan T, Martin W. How many genes in Arabidopsis come from cyanobacteria? An estimate from 386 protein phylogenies. Trends Genet. 2001 Mar;17(3):113–120. [PubMed]
  • Rumpho ME, Summer EJ, Manhart JR. Solar-powered sea slugs. Mollusc/algal chloroplast symbiosis. Plant Physiol. 2000 May;123(1):29–38. [PubMed]
  • Saccone C, Gissi C, Lanave C, Larizza A, Pesole G, Reyes A. Evolution of the mitochondrial genetic system: an overview. Gene. 2000 Dec 30;261(1):153–159. [PubMed]
  • Sandström JP, Russell JA, White JP, Moran NA. Independent origins and horizontal transfer of bacterial symbionts of aphids. Mol Ecol. 2001 Jan;10(1):217–228. [PubMed]
  • Schwartzbach SD, Osafune T, Löffelhardt W. Protein import into cyanelles and complex chloroplasts. Plant Mol Biol. 1998 Sep;38(1-2):247–263. [PubMed]
  • Schyns G, Rippka R, Namane A, Campbell D, Herdman M, Houmard J. Prochlorothrix hollandica PCC 9006: genomic properties of an axenic representative of the chlorophyll a/b-containing oxyphotobacteria. Res Microbiol. 1997 May;148(4):345–354. [PubMed]
  • Selosse M-A, Albert B, Godelle B. Reducing the genome size of organelles favours gene transfer to the nucleus. Trends Ecol Evol. 2001 Mar 1;16(3):135–141. [PubMed]
  • Shigenobu S, Watanabe H, Hattori M, Sakaki Y, Ishikawa H. Genome sequence of the endocellular bacterial symbiont of aphids Buchnera sp. APS. Nature. 2000 Sep 7;407(6800):81–86. [PubMed]
  • Spaulding AW, von Dohlen CD. Psyllid endosymbionts exhibit patterns of co-speciation with hosts and destabilizing substitutions in ribosomal RNA. Insect Mol Biol. 2001 Feb;10(1):57–67. [PubMed]
  • Steiner Jürgen M, Löffelhardt Wolfgang. Protein import into cyanelles. Trends Plant Sci. 2002 Feb;7(2):72–77. [PubMed]
  • Stiller JW, Riley J, Hall BD. Are red algae plants? A critical evaluation of three key molecular data sets. J Mol Evol. 2001 Jun;52(6):527–539. [PubMed]
  • Stoebe B, Kowallik KV. Gene-cluster analysis in chloroplast genomics. Trends Genet. 1999 Sep;15(9):344–347. [PubMed]
  • Surpin Marci, Larkin Robert M, Chory Joanne. Signal transduction between the chloroplast and the nucleus. Plant Cell. 2002;14 (Suppl):S327–S338. [PubMed]
  • Thao ML, Moran NA, Abbot P, Brennan EB, Burckhardt DH, Baumann P. Cospeciation of psyllids and their primary prokaryotic endosymbionts. Appl Environ Microbiol. 2000 Jul;66(7):2898–2905. [PMC free article] [PubMed]
  • Thao ML, Clark MA, Baumann L, Brennan EB, Moran NA, Baumann P. Secondary endosymbionts of psyllids have been acquired multiple times. Curr Microbiol. 2000 Oct;41(4):300–304. [PubMed]
  • Ting Claire S, Rocap Gabrielle, King Jonathan, Chisholm Sallie W. Cyanobacterial photosynthesis in the oceans: the origins and significance of divergent light-harvesting strategies. Trends Microbiol. 2002 Mar;10(3):134–142. [PubMed]
  • Tomitani A, Okada K, Miyashita H, Matthijs HC, Ohno T, Tanaka A. Chlorophyll b and phycobilins in the common ancestor of cyanobacteria and chloroplasts. Nature. 1999 Jul 8;400(6740):159–162. [PubMed]
  • Turner S, Pryer KM, Miao VP, Palmer JD. Investigating deep phylogenetic relationships among cyanobacteria and plastids by small subunit rRNA sequence analysis. J Eukaryot Microbiol. 1999 Jul-Aug;46(4):327–338. [PubMed]
  • Wernegreen JJ, Ochman H, Jones IB, Moran NA. Decoupling of genome size and sequence divergence in a symbiotic bacterium. J Bacteriol. 2000 Jul;182(13):3867–3869. [PMC free article] [PubMed]
  • Whitney SM, Shaw DC, Yellowlees D. Evidence that some dinoflagellates contain a ribulose-1,5-bisphosphate carboxylase/oxygenase related to that of the alpha-proteobacteria. Proc Biol Sci. 1995 Mar 22;259(1356):271–275. [PubMed]
  • Zerges W. Translation in chloroplasts. Biochimie. 2000 Jun-Jul;82(6-7):583–601. [PubMed]
  • Zerges William. Does complexity constrain organelle evolution? Trends Plant Sci. 2002 Apr;7(4):175–182. [PubMed]

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