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How Likely Are We? Evolution of Organismal Complexity

  • William Bains
Chapter

Abstract

All complex multicellular organisms are eukaryotes. How did the evolution of the highly complex architecture of the eukaryotic cell arise? I discuss the differences between bacteria and archaea (prokaryotes) and eukaryotes in terms of chemistry, cellular structure, energetic and genetics. Chemistry and cell structure are less diagnostic of eukaryote than they appear at first. I focus on two pivotal differences between eukaryotes and other forms of life: energetics and genetic control. Eukaryotes can generate substantially more energy per gene than prokaryotes, and this has been suggested as the key enabler of complex genetics. I suggest that a more basic difference is the genetic logic of eukaryotes (not the genetic chemistry, which is shared with all domains of life). Eukaryotic genes are by default ‘off’, prokaryotic ones by default ‘on’. This difference makes growth in genome complexity easier, and growth in control complexity itself then drives a requirement for mitochondria and increased energy production. I conclude that, given ‘default off’ genetics, complex life is highly likely to evolve. The paths to the evolution of ‘default off’ genetics remain to be explored.

Keywords

Sialic Acid Multicellular Organism Genome Complexity Prokaryotic Cell Linear Chromosome 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgements

I am very grateful to my colleague Dirk Schulze-Makuch (Washington State University, WA, USA, and Technical University, Berlin) for our work together on the major steps to complex life. I am also grateful to Janusz Petkowski (MIT, MA, USA) for many helpful comments, to Sara Seager (MIT, MA, USA) for her unfailing and generous support in this and other work, and to Pierre Pontarotti (Ai-Marseilles University, France) and the staff and attendees of the 19th Evolutionary Biology Meeting (Marseilles, France, September 2015) for encouraging me to order my thoughts on why any of us are here at all.

References

  1. Angata T, Varki A (2002) Chemical diversity in the sialic acids and related α-keto acids: an evolutionary perspective. Chem Rev 102(2):439–470. doi: 10.1021/cr000407m PubMedCrossRefGoogle Scholar
  2. Angert ER (2012) DNA replication and genomic architecture of very large bacteria. Ann Rev Microbiol 66(1):197–212. doi: 10.1146/annurev-micro-090110-102827
  3. Angert ER, Clements KD, Pace NR (1993) The largest bacterium. Nature 362(6417):239–241PubMedCrossRefGoogle Scholar
  4. Antonio M, Schulze-Makuch D (2012) Toward a new understanding of multicellularity 2, 1Google Scholar
  5. Bains W, Schulze-Makuch D (2015) Mechanisms of evolutionary innovation point to genetic control logic as the key difference between prokaryotes and eukaryotes. J Mol Evol:1–20. doi: 10.1007/s00239-00015-09688-00236). doi: 10.1007/s00239-015-9688-6
  6. Bains W, Xiao Y, Yu C (2015) Prediction of the maximum temperature for life based on the stability of metabolites to decomposition in water. Life 2:1054–1100CrossRefGoogle Scholar
  7. Baliga NS, Goo YA, Ng WV, Hood L, Daniels CJ, DasSarma S (2000) Is gene expression in Halobacterium NRC-1 regulated by multiple TBP and TFB transcription factors? Mol Microbiol 36(5):1184–1185. doi: 10.1046/j.1365-2958.2000.01916.x PubMedCrossRefGoogle Scholar
  8. Battesti A, Gottesman S (2013) Roles of adaptor proteins in regulation of bacterial proteolysis. Curr Opin Microbiol 16(2):140–147. doi: 10.1016/j.mib.2013.01.002 PubMedPubMedCentralCrossRefGoogle Scholar
  9. Bell SD, Jackson SP (2001) Mechanism and regulation of transcription in archaea. Curr Opin Microbiol 4(2):208–213. doi: 10.1016/S1369-5274(00)00190-9 PubMedCrossRefGoogle Scholar
  10. Bentkowski P, Van Oosterhout C, Mock T (2015) A model of genome size evolution for prokaryotes in stable and fluctuating environments. Genome Biol Evol 7(8):2344–2351. doi: 10.1093/gbe/evv148 PubMedPubMedCentralCrossRefGoogle Scholar
  11. Bonner JT (2004) Perspective: the size-complexity rule. Evolution 58(9):1883–1890. doi: 10.1111/j.0014-3820.2004.tb00476.x PubMedCrossRefGoogle Scholar
  12. Booth A, Doolittle WF (2015) Reply to Lane and Martin: being and becoming eukaryotes. Proc Natl Acad Sci 112(35):E4824. doi: 10.1073/pnas.1513285112 PubMedPubMedCentralCrossRefGoogle Scholar
  13. Cao X, Aufsatz W, Zilberman D, Mette MF, Huang MS, Matzke M, Jacobsen SE (2003) Role of the DRM and CMT3 Methyltransferases in RNA-Directed DNA methylation. Curr Biol 13(24):2212–2217. doi: 10.1016/j.cub.2003.11.052 PubMedCrossRefGoogle Scholar
  14. Cavalier-Smith T (2013) Symbiogenesis: mechanisms, evolutionary consequences, and systematic implications. Ann Rev Ecol Evol Syst 44(1):145–172. doi: 10.1146/annurev-ecolsys-110411-160320
  15. Chan SW-L, Ziberman D, Xie Z, Johansen LK, Carrington JC, Jacobsen SE (2004) RNA silencing genes control de Novo DNA methylation. Science 303:1336PubMedCrossRefGoogle Scholar
  16. Cowan DA (2004) The upper temperature for life—where do we draw the line? Trends Microbiol 12(2):58–60CrossRefGoogle Scholar
  17. de Sousa R, António M, Schulze-Makuch D (2012) Toward a new understanding of multicellularity. Hypotheses Life Sci 2(1):4–14Google Scholar
  18. Dolan MF (2001) Speciation of termite gut protists: the role of bacterial symbionts. Int Microbiol 4(4):203–208PubMedCrossRefGoogle Scholar
  19. Drlica K, Rouviere-Yaniv J (1987) Histonelike proteins of bacteria. Microbiol Rev 51(3):301–319PubMedPubMedCentralGoogle Scholar
  20. Dumesic Phillip A, Natarajan P, Chen C, Drinnenberg Ines A, Schiller Benjamin J, Thompson J, Moresco James J, Yates Iii John R, Bartel David P, Madhani Hiten D (2013) Stalled spliceosomes are a signal for RNAi-mediated genome defense. Cell 152(5):957–968. doi: 10.1016/j.cell.2013.01.046 PubMedPubMedCentralCrossRefGoogle Scholar
  21. Edgell D, Chalamcharla V, Belfort M (2011) Learning to live together: mutualism between self-splicing introns and their hosts. BMC Biol 9(1):22PubMedPubMedCentralCrossRefGoogle Scholar
  22. Elliott TA, Gregory TR (2015) What’s in a genome? The C-value enigma and the evolution of eukaryotic genome content. Philos Trans R Soc Lon B: Biol Sci 370 (1678). doi: 10.1098/rstb.2014.0331
  23. Erickson HP (1997) FtsZ, a tubulin homologue in prokaryote cell division. Trends Cell Biol 7(9):362–367. doi: 10.1016/S0962-8924(97)01108-2 PubMedCrossRefGoogle Scholar
  24. Ferdows MS, Barbour AG (1989) Megabase-sized linear DNA in the bacterium Borrelia burgdorferi, the Lyme disease agent. Proc Natl Acad Sci 86(15):5969–5973PubMedPubMedCentralCrossRefGoogle Scholar
  25. Fuerst JA (2005) Intracellular compartmentalization in Planctomycetes. Ann Rev Microbiol 59:299–328CrossRefGoogle Scholar
  26. Fuerst JA, Webb RI, Garson MJ, Hardy L, Reiswig HM (1998) Membrane-bounded nucleoids in microbial symbionts of marine sponges. FEMS Microbiol Lett 166(1):29–34. doi: 10.1111/j.1574-6968.1998.tb13179.x CrossRefGoogle Scholar
  27. Fusetani N (2012) Marine natural products. In: Civjan N (ed) Natural products in chemical biology. Wiley, Hoboken, pp 31–64CrossRefGoogle Scholar
  28. Gaspin C, Cavaillé J, Erauso G, Bachellerie J-P (2000) Archaeal homologs of eukaryotic methylation guide small nucleolar RNAs: lessons from the Pyrococcus genomes. J Mol Biol 297(4):895–906. doi: 10.1006/jmbi.2000.3593 PubMedCrossRefGoogle Scholar
  29. Geisler S, Coller J (2013) RNA in unexpected places: long non-coding RNA functions in diverse cellular contexts. Nat Rev Mol Cell Biol 14(11):699–712. doi: 10.1038/nrm3679 PubMedPubMedCentralCrossRefGoogle Scholar
  30. Geng F, Wenzel S, Tansey WP, Tansey WP (2012) Ubiquitin and proteasomes in transcription. Ann Rev Biochem 81:177–201PubMedPubMedCentralCrossRefGoogle Scholar
  31. Griese M, Lange C, Soppa J (2011) Ploidy in cyanobacteria. FEMS Microbiol Lett 323(2):124–131PubMedCrossRefGoogle Scholar
  32. Guieysse B, Wuertz S (2012) Metabolically versatile large-genome prokaryotes. Curr Opin Biotechnol 23(3):467–473. doi: 10.1016/j.copbio.2011.12.022 PubMedCrossRefGoogle Scholar
  33. Gunatilaka AL (2012) Plant natural products. In: Civjan N (ed) Natural products in chemical biology. Wiley, Hoboken, pp 3–29Google Scholar
  34. Guttman M, Garber M, Levin JZ, Donaghey J, Robinson J, Adiconis X, Fan L, Koziol MJ, Gnirke A, Nusbaum C, Rinn JL, Lander ES, Regev A (2010) Ab initio reconstruction of cell type-specific transcriptomes in mouse reveals the conserved multi-exonic structure of lincRNAs. Nat Biotech 28 (5):503–510. doi:http://www.nature.com/nbt/journal/v28/n5/abs/nbt.1633.html#supplementary-information
  35. Helmann JD, Chamberlin MJ (1988) Structure and function of bacterial sigma factors. Annu Rev Biochem 57(1):839–872. doi: 10.1146/annurev.bi.57.070188.004203 PubMedCrossRefGoogle Scholar
  36. Hinnebusch J, Tilly K (1993) Linear plasmids and chromosomes in bacteria. Mol Microbiol 10(5):917–922. doi: 10.1111/j.1365-2958.1993.tb00963.x PubMedCrossRefGoogle Scholar
  37. Jacob F, Monod J (1961) On the regulation of gene activity. Cold Spring Harb Symp Quant Biol 26:193–211. doi: 10.1101/sqb.1961.026.01.024 CrossRefGoogle Scholar
  38. Javor B (2012) Hypersaline environments: microbiology and biogeochemistry. Springer, BerlinGoogle Scholar
  39. Kapranov P, Cheng J, Dike S, Nix DA, Duttagupta R, Willingham AT, Stadler PF, Hertel J, Hackermüller J, Hofacker IL, Bell I, Cheung E, Drenkow J, Dumais E, Patel S, Helt G, Ganesh M, Ghosh S, Piccolboni A, Sementchenko V, Tammana H, Gingeras TR (2007) RNA maps reveal new RNA classes and a possible function for pervasive transcription. Science 316(5830):1484–1488. doi: 10.1126/science.1138341 PubMedCrossRefGoogle Scholar
  40. Karin M, Hunter T (1995) Transcriptional control by protein phosphorylation: signal transmission from the cell surface to the nucleus. Curr Biol 5(7):747–757. doi: 10.1016/S0960-9822(95)00151-5 PubMedCrossRefGoogle Scholar
  41. Kireeva ML, Walter W, Tchernajenko V, Bondarenko V, Kashlev M, Studitsky VM (2002) Nucleosome remodeling induced by RNA polymerase II: loss of the H2A/H2B dimer during transcription. Mol Cell 9(3):541–552. doi: 10.1016/S1097-2765(02)00472-0 PubMedCrossRefGoogle Scholar
  42. Knoll AH (2011) The multiple origins of complex multicellularity. Ann Rev Earth Planet Sci 39(1):217–239. doi: 10.1146/annurev.earth.031208.100209
  43. Knoll AH, Hewitt D (2011) Phylogenetic, functional and geological perspectives on complex multicellularity. In: Chalcott B, Sterelny K (eds) The major transitions in evolution revisited. MIT Press, Cambridge, pp 251–270CrossRefGoogle Scholar
  44. Komaki K, Ishikawa H (2000) Genomic copy number of intracellular bacterial symbionts of aphids varies in response to developmental stage and morph of their host. Insect Biochem Mol Biol 30(3):253–258. doi: 10.1016/S0965-1748(99)00125-3 PubMedCrossRefGoogle Scholar
  45. Kube M, Schneider B, Kuhl H, Dandekar T, Heitmann K, Migdoll A, Reinhardt R, Seemuller E (2008) The linear chromosome of the plant-pathogenic mycoplasma ‘Candidatus Phytoplasma mali’. BMC Genom 9(1):306CrossRefGoogle Scholar
  46. Kulp A, Kuehn MJ (2010) Biological functions and biogenesis of secreted bacterial outer membrane vesicles. Annu Rev Microbiol 64:163–184. doi: 10.1146/annurev.micro.091208.073413 PubMedPubMedCentralCrossRefGoogle Scholar
  47. Kumar S, Cheng X, Klimasauskas S, Mi S, Posfai J, Roberts RJ, Wilson GG (1994) The DNA (cytosine-5) methyltransferases. Nucleic Acids Res 22(1):1–10PubMedPubMedCentralCrossRefGoogle Scholar
  48. Landenmark HKE, Forgan DH, Cockell CS (2015) An estimate of the total DNA in the biosphere. PLoS Biol 13(6):e1002168PubMedPubMedCentralCrossRefGoogle Scholar
  49. Lander et al (2001) Initial sequencing and analysis of the human genome. Nature 409(6822):860–921. doi:http://www.nature.com/nature/journal/v409/n6822/suppinfo/409860a0_S1.html
  50. Lane N (2011) Energetics and genetics across the prokaryote-eukaryote divide. Biol Direct 6:35PubMedPubMedCentralCrossRefGoogle Scholar
  51. Lane N, Martin W (2010) The energetics of genome complexity. Nature 467(7318):929–934PubMedCrossRefGoogle Scholar
  52. Lane N, Martin WF (2015) Eukaryotes really are special, and mitochondria are why. Proc Natl Acad Sci 112(35):E4823. doi: 10.1073/pnas.1509237112 PubMedPubMedCentralCrossRefGoogle Scholar
  53. Lane N, Martin WF (2016) Mitochondria, complexity, and evolutionary deficit spending. Proc Natl Acad Sci 113(6):E666. doi: 10.1073/pnas.1522213113 PubMedPubMedCentralCrossRefGoogle Scholar
  54. Livny J, Brencic A, Lory S, Waldor MK (2006) Identification of 17 Pseudomonas aeruginosa sRNAs and prediction of sRNA-encoding genes in 10 diverse pathogens using the bioinformatic tool sRNAPredict2. Nucleic Acids Res 34(12):3484–3493. doi: 10.1093/nar/gkl453 PubMedPubMedCentralCrossRefGoogle Scholar
  55. Lloyd D, Ralphs JR, Harris JC (2002) Giardia intestinalis, a eukaryote without hydrogenosomes, produces hydrogen. Microbiology 148(3):727–733. doi: 10.1099/00221287-148-3-727
  56. Lodé T (2012) For quite a few chromosomes more: the origin of eukaryotes…. J Mol Biol 423(2):135–142. doi: 10.1016/j.jmb.2012.07.005 PubMedCrossRefGoogle Scholar
  57. Lu P, Vogel C, Wang R, Yao X, Marcotte EM (2007) Absolute protein expression profiling estimates the relative contributions of transcriptional and translational regulation. Nat Biotech 25(1):117–124. doi: 10.1038/nbt1270 CrossRefGoogle Scholar
  58. Luijsterburg MS, White MF, Van Driel R, Dame RT (2008) The major architects of chromatin: architectural proteins in bacteria, archaea and eukaryotes. Crit Rev Biochem Mol Biol 43:1–26CrossRefGoogle Scholar
  59. Lynch M, Marinov GK (2015) The bioenergetic costs of a gene. Proc Natl Acad Sci 112(51):15690–15695. doi: 10.1073/pnas.1514974112 PubMedPubMedCentralGoogle Scholar
  60. Lynch M, Marinov GK (2016) Reply to Lane and Martin: mitochondria do not boost the bioenergetic capacity of eukaryotic cells. Proc Natl Acad Sci 113(6):E667–E668. doi: 10.1073/pnas.1523394113 PubMedPubMedCentralCrossRefGoogle Scholar
  61. Makarieva AM, Gorshkov VG, Li B-L, Chown SL, Reich PB, Gavrilov VM (2008) Mean mass-specific metabolic rates are strikingly similar across life’s major domains: evidence for life’s metabolic optimum. Proc Natl Acad Sci 105(44):16994–16999. doi: 10.1073/pnas.0802148105 PubMedPubMedCentralCrossRefGoogle Scholar
  62. Marin B, M. Nowack EC, Melkonian M (2005) A plastid in the making: evidence for a second primary endosymbiosis. Protist 156(4):425–432. doi:http://dx.doi.org/10.1016/j.protis.2005.09.001
  63. Mariscal C, Doolittle WF (2015) Eukaryotes first: how could that be? Phil Trans Roy Soc B 370:20140322CrossRefGoogle Scholar
  64. Martin WF (2011) Early evolution without a tree of life. Biol Direct 6:36PubMedPubMedCentralCrossRefGoogle Scholar
  65. Martin W, Koonin EV (2006) Introns and the origin of nucleus–cytosol compartmentalization. Nature 440:41–45PubMedCrossRefGoogle Scholar
  66. Martin WF, Garg S, Zimorski V (2015) Endosymbiotic theories for eukaryote origin. Philos Trans R Soc Lon B: Biol Sci 370 (1678). doi: 10.1098/rstb.2014.0330
  67. Mattick JS, Makunin IV (2006) Non-coding RNA. Hum Mol Genet 15(suppl 1):R17–R29. doi: 10.1093/hmg/ddl046 PubMedCrossRefGoogle Scholar
  68. Maynard Smith J, Szathmary E (1995) The major transitions in evolution. WH Freeman, OxfordGoogle Scholar
  69. McCutcheon JP, Moran NA (2012) Extreme genome reduction in symbiotic bacteria. Nat Rev Microbiol 10:13–26Google Scholar
  70. McGuire M (2015) Protein kinases. Current progress CALLISTO REFERENCENY, New YorkGoogle Scholar
  71. Mendell JE, Clements KD, Choat JH, Angert ER (2008) Extreme polyploidy in a large bacterium. Proc Natl Acad Sci 105(18):6730–6734. doi: 10.1073/pnas.0707522105 PubMedPubMedCentralCrossRefGoogle Scholar
  72. Miller G, Hahn S (2006) A DNA-tethered cleavage probe reveals the path for promoter DNA in the yeast preinitiation complex. Nat Struct Mol Biol 13(7):603–610. doi:http://www.nature.com/nsmb/journal/v13/n7/suppinfo/nsmb1117_S1.html
  73. Mizuguchi G, Shen X, Landry J, Wu W-H, Sen S, Wu C (2004) ATP-driven exchange of histone H2AZ variant catalyzed by SWR1 chromatin remodeling complex. Science 303(5656):343–348. doi: 10.1126/science.1090701 PubMedCrossRefGoogle Scholar
  74. Moens S, Vanderleyden J (1997) Glycoproteins in prokaryotes. Arch Microbiol 168(3):169–175. doi: 10.1007/s002030050484 PubMedCrossRefGoogle Scholar
  75. Montgomery WL, Pollak PE (1988) Epulopiscium fishelsoni N. G., N. Sp., a protist of uncertain taxonomic affinities from the gut of an herbivorous reef fish. Eukaryot Microbiol 35(4):565–569Google Scholar
  76. Moran NA, McCutcheon JP, Nakabachi A (2008) Genomics and evolution of heritable bacterial symbionts. Ann Rev Genet 42:165–190PubMedCrossRefGoogle Scholar
  77. Müller M, Mentel M, van Hellemond JJ, Henze K, Woehle C, Gould SB, Yu R-Y, van der Giezen M, Tielens AGM, Martin WF (2012) Biochemistry and evolution of anaerobic energy metabolism in eukaryotes. Microbiol Mol Biol Rev 76(2):444–495. doi: 10.1128/mmbr.05024-11 PubMedPubMedCentralCrossRefGoogle Scholar
  78. Nagamune K, Xiong L, Chini E, Sibley LD (2008) Plants, endosymbionts and parasites. Communicative Integr Biol 1(1):62–65. doi: 10.4161/cib.1.1.6106 CrossRefGoogle Scholar
  79. Nagano T, Fraser P (2011) No-nonsense functions for long noncoding RNAs. Cell 145:178–181PubMedCrossRefGoogle Scholar
  80. Navarre WW, Porwollik S, Wang Y, McClelland M, Rosen H, Libby SJ, Fang FC (2006) Selective silencing of foreign DNA with low GC content by the H-NS protein in salmonella. Science 313(5784):236–238. doi: 10.1126/science.1128794 PubMedCrossRefGoogle Scholar
  81. Navarre WW, McClelland M, Libby SJ, Fang FC (2007) Silencing of xenogeneic DNA by H-NS—facilitation of lateral gene transfer in bacteria by a defense system that recognizes foreign DNA. Genes Dev 21(12):1456–1471. doi: 10.1101/gad.1543107 PubMedCrossRefGoogle Scholar
  82. Nechaev S, Adelman K (2011) Pol II waiting in the starting gates: regulating the transition from transcription initiation into productive elongation. Biochim et Biophys Acta (BBA)—Gene Regul Mech 1809(1):34–45. doi:http://dx.doi.org/10.1016/j.bbagrm.2010.11.001
  83. Necsulea A, Soumillon M, Warnefors M, Liechti A, Daish T, Zeller U, Baker JC, Grutzner F, Kaessmann H (2014) The evolution of lncRNA repertoires and expression patterns in tetrapods. Nature 505 (7485):635–640. doi: 10.1038/nature12943. http://www.nature.com/nature/journal/v505/n7485/abs/nature12943.html#supplementary-information
  84. Norris V, Turnock G, Sigee D (1996) The escherichia coli enzoskeleton. Mol Microbiol 19(2):197–204. doi: 10.1046/j.1365-2958.1996.373899.x PubMedCrossRefGoogle Scholar
  85. Olave IA, Peck-Peterson SI, Crabtree GR (2002) Nuclear actin and actin-related proteins in chromatin remodelling. Ann Rev Biochem 71:755–781PubMedCrossRefGoogle Scholar
  86. Ørom UA, Derrien T, Beringer M, Gumireddy K, Gardini A, Bussotti G, Lai F, Zytnicki M, Notredame C, Huang Q, Guigo R, Shiekhattar R (2010) Long noncoding RNAs with enhancer-like function in human cells. Cell 143(1):46–58. doi: 10.1016/j.cell.2010.09.001 PubMedPubMedCentralCrossRefGoogle Scholar
  87. Pickart CM (2001) Mechanisms underlying ubiquitination. Ann Rev. Biochem 70:503–533CrossRefGoogle Scholar
  88. Pittis AA, Gabaldón T (2016) Late acquisition of mitochondria by a host with chimaeric prokaryotic ancestry. Nat Adv Online Publication. doi: 10.1038/nature16941. http://www.nature.com/nature/journal/vaop/ncurrent/abs/nature16941.html#supplementary-information
  89. Ponting CP, Oliver PL, Reik W (2009) Evolution and functions of long noncoding RNAs. Cell 136(4):629–641. doi: 10.1016/j.cell.2009.02.006 PubMedCrossRefGoogle Scholar
  90. Pyle AM (2012) Group II intron architecture and its implications for the development of eukaryotic splicing systems. FASEB J 26(217):213Google Scholar
  91. Reyes-Prieto A, Yoon HS, Moustafa A, Yang EC, Andersen RA, Boo SM, Nakayama T, K-i Ishida, Bhattacharya D (2010) Differential gene retention in plastids of common recent origin. Mol Biol Evol 27(7):1530–1537. doi: 10.1093/molbev/msq032 PubMedPubMedCentralCrossRefGoogle Scholar
  92. Rhee HS, Pugh F (2012) Genome-wide structure and organization of eukaryotic pre-initiation complexes. Nature 483:295–301PubMedPubMedCentralCrossRefGoogle Scholar
  93. Rivas E, Klein RJ, Jones TA, Eddy SR (2001) Computational identification of noncoding RNAs in E. coli by comparative genomics. Curr Biol 11(17):1369–1373. doi: 10.1016/S0960-9822(01)00401-8 PubMedCrossRefGoogle Scholar
  94. Roeben A, Kofler C, Nagy I, Nickell S, Ulrich Hartl F, Bracher A (2006) Crystal structure of an archaeal actin homolog. J Mol Biol 358(1):145–156. doi: 10.1016/j.jmb.2006.01.096 PubMedCrossRefGoogle Scholar
  95. Rokas A (2008) The origins of multicellularity and the early history of the genetic toolkit for animal development. Ann Rev Genet 42(1):235–251. doi: 10.1146/annurev.genet.42.110807.091513
  96. Roy SW, Gilbert W (2006) The evolution of spliceosomal introns: patterns, puzzles and progress. Nat Rev Genet 7:211–221PubMedGoogle Scholar
  97. Sanchez S, Guzman-Trampe S, Avalos M, Ruiz B, Rodriguez-Sanoja R, Jim´enez-Estrada M (2012) Bacterial natural products. In: Civjan N (ed) Natural products in chemical biology. Wiley, Hoboken, pp 65–108Google Scholar
  98. Sandman K, Reeve JN (2001) Chromosome packaging by archael histones. In: Laskin AL, Bennett JW, Gadd gM (eds) Advances in applied microbiology, vol 50. Academic Press, San Diego, pp 73–100Google Scholar
  99. Sandman K, Reeve JN (2005) Archaeal chromatin proteins: different structures but common function? Curr Opin Microbiol 8(6):656–661. doi: 10.1016/j.mib.2005.10.007 PubMedCrossRefGoogle Scholar
  100. Sassera D, Beninati T, Bandi C, Bouman EAP, Sacchi L, Fabbi M, Lo N (2006) ‘Candidatus Midichloria mitochondrii’, an endosymbiont of the tick Ixodes ricinus with a unique intramitochondrial lifestyle. Int J Syst Evol Microbiol 56(11):2535–2540. doi: 10.1099/ijs.0.64386-0 PubMedCrossRefGoogle Scholar
  101. Schulz HN, Brinkhoff T, Ferdelman TG, Mariné MH, Teske A, Jørgensen BB (1999) Dense populations of a giant sulfur bacterium in namibian shelf sediments. Science 284(5413):493–495. doi: 10.1126/science.284.5413.493 PubMedCrossRefGoogle Scholar
  102. Shen X, Mizuguchi G, Hamiche A, Wu C (2000) A chromatin remodelling complex involved in transcription and DNA processing. Nature 406 (6795):541–544. doi:http://www.nature.com/nature/journal/v406/n6795/suppinfo/406541A0_S1.html
  103. Sherman L, Min H, Toepel J, Pakrasi H (2010) Better living through cyanothece—unicellular diazotrophic cyanobacteria with highly versatile metabolic systems. In: Hallenbeck PC (ed) Recent advances in phototrophic prokaryotes, vol 675. Advances in experimental medicine and biology. Springer New York, pp 275–290. doi: 10.1007/978-1-4419-1528-3_16
  104. Soppa J (2010) Protein acetylation in archaea, bacteria, and eukaryotes. Archaea. doi: 10.1155/2010/820681
  105. Soppa J (2014) Polyploidy in archaea and bacteria: about desiccation resistance, giant cell size, long-term survival, enforcement by a eukaryotic host and additional aspects. J Mol Microbiol Biotechnol 24(5–6):409–419PubMedGoogle Scholar
  106. Spang A, Saw JH, Jorgensen SL, Zaremba-Niedzwiedzka K, Martijn J, Lind AE, van Eijk R, Schleper C, Guy L, Ettema TJG (2015) Complex archaea that bridge the gap between prokaryotes and eukaryotes. Nature 521(7551):173–179. doi: 10.1038/nature14447. http://www.nature.com/nature/journal/v521/n7551/abs/nature14447.html#supplementary-information
  107. Stolz JF (2001) Bacterial intracellular membranes. In: eLS. Wiley. doi: 10.1002/9780470015902.a0000303.pub2
  108. Szathmáry E (2015) Toward major evolutionary transitions theory 2.0. Proc Natl Acad Sci 112(33):10104–10111. doi: 10.1073/pnas.1421398112 PubMedPubMedCentralCrossRefGoogle Scholar
  109. Thao ML, Gullan PJ, Baumann P (2002) Secondary (γ-Proteobacteria) endosymbionts infect the primary (β-Proteobacteria) endosymbionts of mealybugs multiple times and coevolve with their hosts. Appl Environ Microbiol 68(7):3190–3197. doi: 10.1128/aem.68.7.3190-3197.2002 PubMedPubMedCentralCrossRefGoogle Scholar
  110. Tirichine L, Bowler C (2011) Decoding algal genomes: tracing back the history of photosynthetic life on Earth. Plant J 66:45–57PubMedCrossRefGoogle Scholar
  111. Ulitsky I, Shkumatava A, Jan Calvin H, Sive H, Bartel David P (2011) Conserved function of lincRNAs in vertebrate embryonic development despite rapid sequence evolution. Cell 147(7):1537–1550. doi: 10.1016/j.cell.2011.11.055 PubMedPubMedCentralCrossRefGoogle Scholar
  112. van Der Giezen M (2009) Hydrogenosomes and mitosomes: conservation and evolution of functions. J Eukaryot Microbiol 56(3):221–231PubMedCrossRefGoogle Scholar
  113. van der Giezen M, Tovar J (2005) Degenerate mitochondria. EMBO Rep 6(6):525–530. doi: 10.1038/sj.embor.7400440 PubMedPubMedCentralCrossRefGoogle Scholar
  114. Varki A, Schauer R (2009) Sialic acidsGoogle Scholar
  115. Venter et al (2001) The sequence of the human genome. Science 291 (5507):1304–1351. doi: 10.1126/science.1058040
  116. Viollier PH, Thanbichler M, McGrath PT, West L, Meewan M, McAdams HH, Shapiro L (2004) Rapid and sequential movement of individual chromosomal loci to specific subcellular locations during bacterial DNA replication. Proc Nat Acad Sci 101 (9257–9262)Google Scholar
  117. Vockenhuber M-P, Sharma CM, Statt MG, Schmidt D, Xu Z, Dietrich S, Liesegang H, Mathews DH, Suess B (2011) Deep sequencing-based identification of small non-coding RNAs in Streptomyces coelicolor. RNA Biol 8(3):468–477PubMedPubMedCentralCrossRefGoogle Scholar
  118. Wardleworth BN, Russell RJM, Bell SD, Taylor GL, White MF (2002) Structure of Alba: an archaeal chromatin protein modulated by acetylation. EMBO J 21(17):4654–4662. doi: 10.1093/emboj/cdf465 PubMedPubMedCentralCrossRefGoogle Scholar
  119. Washietl S, Pedersen JS, Korbel JO, Stocsits C, Gruber AR, Hackermüller J, Hertel J, Lindemeyer M, Reiche K, Tanzer A, Ucla C, Wyss C, Antonarakis SE, Denoeud F, Lagarde J, Drenkow J, Kapranov P, Gingeras TR, Guigó R, Snyder M, Gerstein MB, Reymond A, Hofacker IL, Stadler PF (2007) Structured RNAs in the ENCODE selected regions of the human genome. Genome Res 17(6):852–864. doi: 10.1101/gr.5650707 PubMedPubMedCentralCrossRefGoogle Scholar
  120. Weinzierl ROJ (2013) The RNA polymerase factory and archaeal transcription. Chem Rev 113:8350–8376PubMedCrossRefGoogle Scholar
  121. White MF, Bell SD (2002) Holding it together: chromatin in the Archaea. Trends Genet 18(12):621–626. doi: 10.1016/S0168-9525(02)02808-1 PubMedCrossRefGoogle Scholar
  122. Whitman WB, Coleman DC, Wiebe WJ (1998) Prokaryotes: the unseen majority. Proc Natl Acad Sci 95(12):6578–6583PubMedPubMedCentralCrossRefGoogle Scholar
  123. Wilkins A (2002) The evolution of developmental pathways. Sinauer Associates, SunderlandGoogle Scholar
  124. William RS, Gilbert W (2006) The evolution of spliceosomal introns: patterns, puzzles and progress. Nat Rev Genet 7(3):211–221CrossRefGoogle Scholar
  125. Williams JP, Hallsworth JE (2009) Limits of life in hostile environments: no barriers to biosphere function? Environ Microbiol 11(12):3292–3308. doi: 10.1111/j.1462-2920.2009.02079.x PubMedPubMedCentralCrossRefGoogle Scholar
  126. Williams TA, Foster PG, Cox CJ, Embley TM (2014) An archeal origin of eukaryotes supports only two primary domains of life. Nature 504:231–236CrossRefGoogle Scholar
  127. Woese CR, Kandler O, Wheelis ML (1990) Towards a natural system of organisms: proposal for the domains archaea, bacteria, and eucarya. Proc Natl Acad Sci 87(12):4576–4579. doi: 10.1073/pnas.87.12.4576 PubMedPubMedCentralCrossRefGoogle Scholar
  128. Wujek DE (1979) Intracellular bacteria in the blue-green alga Pleurocapsa minor. Trans Am Microsc Soc 98(1):143–145CrossRefGoogle Scholar
  129. Xie Y, Reeve JN (2004) Transcription by an Archaeal RNA polymerase is slowed but not blocked by an Archaeal nucleosome. J Bacteriol 186(11):3492–3498. doi: 10.1128/jb.186.11.3492-3498.2004
  130. Yutin N, Koonin EV (2012) Archaeal origin of tubulin. Biol Direct 7 (10)Google Scholar
  131. Zerulla K, Soppa J (2014) Polyploidy in haloarchaea: advantages for growth and survival. Front Microbiol 5:274. doi: 10.3389/fmicb.2014.00274 PubMedPubMedCentralCrossRefGoogle Scholar
  132. Zhang A, Rimsky S, Reaban ME, Buc H, Belfort M (1996) Escherichia coli protein analogs StpA and H-NS: regulatory loops, similar and disparate effects on nucleic acid dynamics. EMBO J 15(6):1340–1349PubMedPubMedCentralGoogle Scholar
  133. Zimorski V, Ku C, Martin WF, Gould SB (2014) Endosymbiotic theory for organelle origins. Curr Opin Microbiol 22:38–48. doi: 10.1016/j.mib.2014.09.008 PubMedCrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  1. 1.EAPS MITCambridgeUSA

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