AJMB  Vol.3 No.4 , October 2013
The origin of biological information and programmed protein synthesis
Author(s) Dan Liu*
ABSTRACT
Biological information is one of the most important characteristics of life, and it enables life to evolve to higher complexity and adapt to the environment by mutation and natural selection. However, the origin of this information recording and retrieval system remains a mystery. To understand the origin of biological information will lead us to one step closer to understand the origin of life on earth. Biological information is encoded in DNA and translated into protein by the ribosome in all free living organisms. The information has to be translated into proteins to carry out its biological functions, so the evolution of the ribosome must be integrated with the development of biological information. In this article, I propose that the small ribosomal subunit evolved from a ribozyme that acted as an RNA helicase in the ancient RNA world, and the involvement of tRNAs and the large ribosomal subunit evolved to enhance the helicase activity and to overcome the higher energy require-ment for high GC content RNA helices. This process could have developed as a primitive recording mechanism: since Watson-Crick base paring is a natural property of RNA, each time the proto-small ribosomal subunit came to a particular GC-rich helix, tRNA-like molecules and the proto-large ribosomal subunit would have to be engaged to generate the helicase activity, and consequently the same polypeptide would be synthesized as a by-product. Simple recorded messages then evolved into useful biological information through continuous mutation and natu-ral selection. This hypothesis provides logical and incremental steps for the development of programmed protein synthesis. I also argue that the helicase activity is preserved in the modern ribosome and that from our knowledge of the ribosome, and we can deduce the possible mechanisms of the helicase activity.

Cite this paper
Liu, D. (2013) The origin of biological information and programmed protein synthesis. American Journal of Molecular Biology, 3, 204-214. doi: 10.4236/ajmb.2013.34027.
References
[1]   Crick, F.R. (1968) The origin of genetic code. Journal of Molecular Biology, 38, 367-379.
http://dx.doi.org/10.1016/0022-2836(68)90392-6

[2]   Gilbert, W. (1986) The RNA world. Nature, 319, 618. http://dx.doi.org/10.1038/319618a0

[3]   Noller, H. (2004) The driving force for molecular evolution of transloation. RNA, 10, 1833-1837.
http://dx.doi.org/10.1261/rna.7142404

[4]   Orgel, L.E. (1968) Evolution of the genetic apparatus. Journal of Molecular Biology, 38, 381-393.
http://dx.doi.org/10.1016/0022-2836(68)90393-8

[5]   Wolf, Y.I. and Koonin, E.V. (2007) On the origin of the translation system and genetic code in the RNA world by means of natural selection, exaptation, and subfunctionalisztion. Biology Direct, 2, 14-39.
http://dx.doi.org/10.1186/1745-6150-2-14

[6]   Dorner, S., Brunelle, J.L., Sharma, D. and Green, R. (2006) The hybrid state of tRNA binding is an authentic translation elongation intermediate. Nature Structural & Molecular Biology, 13, 234-241.
http://dx.doi.org/10.1038/nsmb1060

[7]   Moazed, D. and Noller, H.F. (1989) Intermediate states in the movement of transfer RNA in the ribosome. Nature, 342, 142-148.
http://dx.doi.org/10.1038/342142a0

[8]   Joseph, S. (2003) After the ribosome structure: How does translocation work? RNA, 9, 160-164.
http://dx.doi.org/10.1261/rna.2163103

[9]   Korostelev, A., Ermolenko, D.N. and Noller, H.F. (2008) Structural dynamics of the ribosome. Current Opinion in Chemical Biology, 12, 674-683.
http://dx.doi.org/10.1016/j.cbpa.2008.08.037

[10]   Woese, C. (1970) Molecular mechanics of translation: A reciprocating ratchet mechanism. Nature, 226, 817-820.
http://dx.doi.org/10.1038/226817a0

[11]   Noller, H.F. (1993) On the origin of the ribosome: Coevolution of subdomains of tRNA and rRNA. In: Gesteland, R.F. and Atkins, J.F. Eds., The RNA world, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York, 137-156.

[12]   Poole, A.M., Jeffares, D.C. and Penny, D. (1998) The path from the RNA world. Journal of Molecular Evolution, 46, 1-17.
http://dx.doi.org/10.1007/PL00006275

[13]   Fox, G.E. and Naik, A.K. (2004) The evolutionary history of the translation machinery. In: De Pouplana, R.L. Ed., The Genetic Code and The Origin of Life, Landers BioScience, Georgetown, 92-105.
http://dx.doi.org/10.1007/0-387-26887-1_6

[14]   Maizels, N. and Weiner, A.M. (1993) The genomic tag hypothesis: Modern viruses as molecular fossils of ancient strategies for genomic replication. In: Gesteland, R.F. and Atkins, J.F., Eds., The RNA world, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York, 577-602.

[15]   Schimmel, P., Giege, R., Moras, D. and Yokoyama, S. (1993) An operational RNA code for amino acids and possible relationship to genetic code. Proceedings of the National Academy of Sciences of the United States of America, 90, 8763-8768.
http://dx.doi.org/10.1073/pnas.90.19.8763

[16]   Agmon, I., Bashan, A. and Yonath, A. (2006) On ribosome conservation and evolution. Israel Journal of Ecology and Evolution, 52, 359-379.
http://dx.doi.org/10.1560/IJEE_52_3-4_359

[17]   Sievers, A., Beringer, M., Rodnina, M.V. and Wolfenden, R. (2004) The ribosome as an entropy trap. Proceedings of the National Academy of Sciences of the United States of America, 101, 7897-7901.
http://dx.doi.org/10.1073/pnas.0402488101

[18]   Bokov, K. and Steinberg, S.V. (2009) A hierarchical model for evolution of 23S ribosomal RNA. Nature, 457, 977-980. http://dx.doi.org/10.1038/nature07749

[19]   Hsiao, C., Mohan, S., Kalahar, B.K. and Williams, L.D. (2009) Peeling the onion: ribosomes are ancient molecular fossils. Molecular Biology and Evolution, 26, 2415-2425. http://dx.doi.org/10.1093/molbev/msp163

[20]   Mzathmary, E. and Smith, M. (1997) From replicators to re-producers: The first major transition leading to life. Journal of Theoretical Biology, 187, 555-571.
http://dx.doi.org/10.1006/jtbi.1996.0389

[21]   Rodin, A.S., Szathmary, E. and Rodin, S.N. (2011) On origin of genetic code and tRNA before translation. Biology Direct, 6, 14.
http://dx.doi.org/10.1186/1745-6150-6-14

[22]   Rodin, A.S., Szathmary, E. and Rodin, S.N. (2009) On ancestor for codes viewed from the perspective of two complementary modes of tRNA aminoacylation. Biology Direct, 4, 4. http://dx.doi.org/10.1186/1745-6150-4-4

[23]   Gordon, K.H.J. (1995) Were RNA replication and translation directly coupled in the RNA (+protein?) world? Journal of Theoretical Biology, 173, 179-193.
http://dx.doi.org/10.1006/jtbi.1995.0054

[24]   Eigen, M. (1971) Selforganization of matter and the evolution of biological macromolecules. Die Naturwissenschaften, 58, 465-523.
http://dx.doi.org/10.1007/BF00623322

[25]   Kun, A., Santos, M. and Szathmary, E. (2005) Real ribozymes suggest a relaxed error threshold. Nature Genetics, 37, 1008-1011.
http://dx.doi.org/10.1038/ng1621

[26]   Fox, G.E. (2010) Origin and evolution of the ribosome. Cold Spring Harbor Perspectives in Biology, 9, a003483.
http://dx.doi.org/10.1101/cshperspect.a003483

[27]   Miller, S.L. (1953) A production of amino acids under possible primitive earth conditions. Science, 117, 528-529. http://dx.doi.org/10.1126/science.117.3046.528

[28]   Travers, A. (2006) The evolution of the genetic code revisited. Origins of Life and Evolution of Biospheres, 36, 549-555. http://dx.doi.org/10.1007/s11084-006-9041-6

[29]   Bultrini, E. and Pizzi, E. (2006) A new parameter to study compositional properties of non-coding regions in eukaryotic genomes. Gene, 385, 75-82.
http://dx.doi.org/10.1016/j.gene.2006.05.030

[30]   Grantham, R., Gautier, C., Gouy, M., Mercier, R. and Pave, A. (1980) Codon catalog usage and the genome hypothesis. Nucleic Acids Research, 8, r49-r62.
http://dx.doi.org/10.1093/nar/8.1.197-c

[31]   Zenkin, N. (2012) Hypothesis: Emergence of translation as a result of RNA helicase evolution. Journal of Molecular Evolution, 74, 249-256.
http://dx.doi.org/10.1007/s00239-012-9503-6

[32]   Takyar, S., Hickerson, R.P. and Noller, H.F. (2005) mRNA helicase activity of the ribosome. Cell, 120, 49-58.
http://dx.doi.org/10.1016/j.cell.2004.11.042

[33]   Fredrick, K. and Noller, H.F. (2003) Catalysis of ribosomal translocation by sparsomycin. Science, 300, 1159-1162.http://dx.doi.org/10.1126/science.1084571

[34]   Wen, J.D., Lancaster, L., Hodges, C., Zeri, A.C., Yoshimura, S.H. and Noller, H.F., et al. (2008) Following translation by single ribosomes one codon at a time. Nature, 452, 598-603.
http://dx.doi.org/10.1038/nature06716

[35]   Qu, X., Wen, J.D., Lancaster, L., Noller, H.F., Bustamante, C. and Tinoco, I. Jr. (2011) The ribosome uses two active mechanisms to unwind messenger RNA during translation. Nature, 475, 118-121.
http://dx.doi.org/10.1038/nature10126

[36]   Ogle, J.M., Brodersen, D.E., Clemons Jr., W.M., Tarry, M.J., Carter, A.P. and Ramakrishnan, V. (2001) Recognition of cognate transfer RNA by the 30S ribosomal subunit. Science, 292, 897-902.
http://dx.doi.org/10.1126/science.1060612

[37]   Berk, V., Zhang, W., Pai, R.D. and Cate, J.H. (2006) Structural basis for mRNA and tRNA positioning on the ribosome. Proceedings of the National Academy of Sciences of the United States of America, 103, 15830-15834.
http://dx.doi.org/10.1073/pnas.0607541103

[38]   Vanzi, F., Takagi, Y., Shuman, H., Cooperman, B.S. and Goldman, Y.E. (2005) Mechanical studies of single ribosome/mRNA complexes. Biophysical Journal, 89, 1909-1919. http://dx.doi.org/10.1529/biophysj.104.056283

[39]   Korostelev, A., Trakhanov, S., Laurberg, M. and Noller, H.F. (2006) Crystal structure of a 70S ribosome-tRNA complex reveals functional interactions and rearrange-ments. Cell, 126, 1065-1077.
http://dx.doi.org/10.1016/j.cell.2006.08.032

[40]   Noller, H.F. and Baucom, A. (2002) Structure of the 70 S ribosome: Implications for movement. Biochemical Society Transactions, 30, 1159-1161.
http://dx.doi.org/10.1042/BST0301159

[41]   Horan, L.H. and Noller, H.F. (2007) Intersubunit movement is required for ribosomal translocation. Proceedings of the National Academy of Sciences of the United States of America, 104, 4881-4885.
http://dx.doi.org/10.1073/pnas.0700762104

[42]   Muldoon-Jacobs, K.L. and Dinman, J.D. (2006) Specific effects of ribosome-tethered molecular chaperones on programmed -1 ribosomal frameshifting. Eukaryotic Cell, 5, 762-770.
http://dx.doi.org/10.1128/EC.5.4.762-770.2006

[43]   Zaher, H.S. and Green, R. (2009) Quality control by the ribosome following peptide bond formation. Nature, 457, 161-166.

[44]   Schuwirth, B.S., Borovinskaya, M.A., Hau, C.W., Zhang, W., Vila-Sanjurjo, A., Holton, J.M., et al. (2005) Structures of the bacterial ribosome at 3.5 A resolution. Science, 310, 827-834.
http://dx.doi.org/10.1126/science.1117230

[45]   Kozak, M. (1978) How do eucaryotic ribosomes select initiation regions in messenger RNA? Cell, 15, 1109-1123. http://dx.doi.org/10.1016/0092-8674(78)90039-9

[46]   Kozak, M. (1989) The scanning model for translation: An update. The Journal of Cell Biology, 108, 229-241.
http://dx.doi.org/10.1083/jcb.108.2.229

[47]   Herr, A.J., Atkins, J.F. and Gesteland, R.F. (1999) Mutations which alter the elbow region of tRNA2Gly reduce T4 gene 60 translational bypassing efficiency. The EMBO Journal, 18, 2886-2896.
http://dx.doi.org/10.1093/emboj/18.10.2886

[48]   Weiss, R.B., Huang, W.M. and Dunn, D.M. (1990) A nascent peptide is required for ribosomal bypass of the coding gap in bacteriophage T4 gene 60. Cell, 62, 117-126. http://dx.doi.org/10.1016/0092-8674(90)90245-A

[49]   Ogle, J.M., Murphy, F.V., Tarry, M.J. and Ramakrishnan, V. (2002) Selection of tRNA by the ribosome requires a transition from an open to a closed form. Cell, 111, 721-732. http://dx.doi.org/10.1016/S0092-8674(02)01086-3

[50]   Selmer, M., Dunham, C.M., Murphy, F.V., Weixlbaumer, A., Petry, S., Kelley, A.C., et al. (2006) Structure of the 70S ribosome complexed with mRNA and tRNA. Science, 313, 1935-1942.
http://dx.doi.org/10.1126/science.1131127

[51]   Cukras, A.R., Southworth, D.R., Brunelle, J.L., Culver, G.M. and Green, R. (2003) Ribosomal proteins S12 and S13 function as control elements for translocation of the mRNA: tRNA complex. Molecular Cell, 12, 321-328.
http://dx.doi.org/10.1016/S1097-2765(03)00275-2

[52]   Southworth, D.R., Brunelle, J.L. and Green, R. (2002) EFG-independent translocation of the mRNA: tRNA complex is promoted by modification of the ribosome with thiol-specific reagents. Journal of Molecular Biology, 324, 611-623.
http://dx.doi.org/10.1016/S0022-2836(02)01196-8

[53]   Pan, D., Kirillov, S.V. and Cooperman, B.S. (2007) Kinetically competent intermediates in the translocation step of protein synthesis. Molecular Cell, 25, 519-529.
http://dx.doi.org/10.1016/j.molcel.2007.01.014

[54]   Spiegel, P.C., Ermolenko, D.N. and Noller, H.F. (2007) Elongation factor G stabilizes the hybrid-state conformation of the 70S ribosome. RNA, 13, 1473-1482.
http://dx.doi.org/10.1261/rna.601507

[55]   Zavialov, A.V., Hauryliuk, V.V. and Ehrenberg, M. (2005) Guanine-nucleotide exchange on ribosome-bound elongation factor G initiates the translocation of tRNAs. Journal of Biology, 4, 9. http://dx.doi.org/10.1186/jbiol24

[56]   Agirrezabala, X., Lei, J., Brunelle, J.L., Ortiz-Meoz, R.F., Green, R. and Frank, J. (2008) Visualization of the hybrid state of tRNA binding promoted by spontaneous ratcheting of the ribosome. Molecular Cell, 32, 190-197.
http://dx.doi.org/10.1016/j.molcel.2008.10.001

[57]   Dunkle, J.A., Wang, L., Feldman, M.B., Pulk, A., Chen, V.B., Kapral, G.J., et al. (2011) Structures of the bacterial ribosome in classical and hybrid states of tRNA binding. Science, 332, 981-984.
http://dx.doi.org/10.1126/science.1202692

[58]   Ermolenko, D.N. and Noller, H.F. (2011) mRNA translocation occurs during the second step of ribosomal intersubunit rotation. Nature Structural & Molecular Biology, 18, 457-462.

[59]   Cornish, P.V., Ermolenko, D.N., Noller, H.F. and Ha, T. (2008) Spontaneous intersubunit rotation in single ribosomes. Molecular Cell, 30, 578-588.
http://dx.doi.org/10.1016/j.molcel.2008.05.004

[60]   Fischer, N., Konevega, A.L., Wintermeyer, W., Rodnina, M.V. and Stark, H. (2010) Ribosome dynamics and tRNA movement by time-resolved electron cryomicroscopy. Nature, 466, 329-333.

[61]   Borovinskaya, M.A., Shoji, S., Holton, J.M., Fredrick, K. and Cate, J.H.D. (2007) A steric block in translation caused by the antibiotic spectinomycin. ACS Chemical Biology, 2, 545-552. http://dx.doi.org/10.1021/cb700100n

[62]   Frank, J. and Agrawal, R.K. (2001) Ratchet-like movements between the two ribosomal subunits: Their implications in elongation factor recognition and tRNA translocation. Cold Spring Harbor Symposia on Quantitative Biology, 66, 67-75.
http://dx.doi.org/10.1101/sqb.2001.66.67

[63]   Julian, P., Konevega, A.L., Scheres, S.H., Lazaro, M., Gil, D., Wintermeyer, W., et al. (2008) Structure of ratcheted ribosomes with tRNAs in hybrid states. Proceedings of the National Academy of Sciences of the United States of America, 105, 16924-16927.
http://dx.doi.org/10.1073/pnas.0809587105

[64]   Namy, O., Moran, S.J., Stuart, D.I., Gilbert, R.J. and Brierley, I. (2006) A mechanical explanation of RNA pseudoknot function in programmed ribosomal frameshifting. Nature, 441, 244-247.

[65]   Gavrilova, L.P., Kostiashkina, O.E., Koteliansky, V.E., Rutkevitch, N.M. and Spirin, A.S. (1976) Factor-free (“non-enzymic”) and factor-dependent systems of translation of polyuridylic acid by Escherichia coli ribosomes. Journal of Molecular Biology, 101, 537-552.
http://dx.doi.org/10.1016/0022-2836(76)90243-6

[66]   Gavrilova, L.P. and Spirin, A.S. (1971) Stimulation of “non-enzymic” translocation in ribosomes by p-chloromercuribenzoate. FEBS Letters, 17, 324-326.
http://dx.doi.org/10.1016/0014-5793(71)80177-1

[67]   Pestka, S. (1974) Assay for nonenzymatic and enzymatic translocation with Escherichia coli ribosomes. Methods in Enzymology, 30, 462-470.
http://dx.doi.org/10.1016/0076-6879(74)30046-8

[68]   Sergiev, P.V., Lesnyak, D.V., Kiparisov, S.V., Burakovsky, D.E., Leonov, A.A., Bogdanov, A.A., et al. (2005) Function of the ribosomal E-site: A mutagenesis study. Nucleic Acids Research, 33, 6048-6056.
http://dx.doi.org/10.1093/nar/gki910

[69]   Walker, S.E., Shoji, S., Pan, D., Cooperman, B.S. and Fredrick, K. (2008) Role of hybrid tRNA-binding states in ribosomal translocation. Proceedings of the National Academy of Sciences of the United States of America, 105, 9192-9197. http://dx.doi.org/10.1073/pnas.0710146105

[70]   Feinberg, J.S. and Joseph, S. (2001) Identification of molecular interactions between P-site tRNA and the ribosome essential for translocation. Proceedings of the National Academy of Sciences of the United States of America, 98, 11120-11125.
http://dx.doi.org/10.1073/pnas.211184098

[71]   Lill, R., Robertson, J.M. and Wintermeyer, W. (1989) Binding of the 3’ terminus of tRNA to 23S rRNA in the ribosomal exit site actively promotes translocation. The EMBO Journal, 8, 3933-3938.

[72]   Virumae, K., Saarma, U., Horowitz, J. and Remme, J. (2002) Functional importance of the 3’-terminal adenosine of tRNA in ribosomal translation. The Journal of Biological Chemistry, 277, 24128-24134.
http://dx.doi.org/10.1074/jbc.M200393200

[73]   Subramanian, A.R. and Dabbs, E.R. (1980) Functional studies on ribosomes lacking protein L1 from mutant Escherichia coli. European Journal of Biochemistry, 112, 425-430. http://dx.doi.org/10.1111/j.1432-1033.1980.tb07222.x

[74]   Uemura, S., Dorywalska, M., Lee, T.H., Kim, H.D., Puglisi, J.D. and Chu, S. (2007) Peptide bond formation destabilizes shine-dalgarno interaction on the ribosome. Nature, 446, 454-457.

[75]   Caetano-Anolles, D., Kim, K.M., Mittenthal, J.E. and Caetano-Anolles, G. (2011) Proteome evolution and the metabolic origins of translation and cellular life. Journal of Molecular Evolution, 72, 14-33.
http://dx.doi.org/10.1007/s00239-010-9400-9

[76]   Caetano-Anolles, G., Kim, K.M. and Caetano-Anolles, D. (2012) The phylogenomic roots of modern biochemistry: Origins of proteins, cofactors and protein biosynthesis. Journal of Molecular Evolution, 74, 1-34.
http://dx.doi.org/10.1007/s00239-011-9480-1

[77]   Harish, A. and Caetano-Anolles, G. (2012) Ribosomal history reveals origins of modern protein synthesis. PloS One, 7, e32776.
http://dx.doi.org/10.1371/journal.pone.0032776

[78]   Bernhardt, H.S. and Tate, W.P. (2010) The transition from noncoded to coded protein synthesis: Did coding mRNAs arise from stability-enhancing binding partners to tRNA? Biology Direct, 5, 16-29.
http://dx.doi.org/10.1186/1745-6150-5-16

[79]   Schafer, M.A., Tastan, A.O., Patzke, S., Blaha, G., Spahn, C.M., Wilson, D.N., et al. (2002) Codon-anticodon interaction at the P site is a prerequisite for tRNA interaction with the small ribosomal subunit. The Journal of Biological Chemistry, 277, 19095-19105.
http://dx.doi.org/10.1074/jbc.M108902200

 
 
Top