Skip to main content
SpringerLink
Log in

Phylogenetic Differences in Content and Intensity of Periodic Proteins

  • Published:
Journal of Molecular Evolution Aims and scope Submit manuscript

Abstract

Many proteins exhibit sequence periodicity, often correlated with a visible structural periodicity. The statistical significance of such periodicity can be assessed by means of a chi-squared-based test, with significance thresholds being calculated from shuffled sequences. Comparison of the complete proteomes of 45 species reveals striking differences in the proportion of periodic proteins and the intensity of the most significant periodicities. Eukaryotes tend to have a higher proportion of periodic proteins than eubacteria, which in turn tend to have more than archaea. The intensity of periodicity in the most periodic proteins is also greatest in eukaryotes. By contrast, the relatively small group of periodic proteins in archaea also tend to be weakly periodic compared to those of eukaryotes and eubacteria. Exceptions to this general rule are found in those prokaryotes with multicellular life-cycle phases, e.g., Methanosarcina sp., or Anabaena sp., which have more periodicities than prokaryotes in general, and in unicellular eukaryotes, which have fewer than multicellular eukaryotes. The distribution of significantly periodic proteins in eukaryotes is over a wide range of period lengths, whereas prokaryotic proteins typically have a more limited set of period lengths. This is further investigated by repeating the analysis on the NRL-3D database of proteins of solved structure. Some short-range periodicities are explicable in terms of basic secondary structure, e.g., alpha helices, while middle-range periodicities are frequently found to consist of known short Pfam domains, e.g., leucine-rich repeats, tetratricopeptides or armadillo domains. However, not all can be explained in this way.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Figure 1
Figure 2
Figure 3
Figure 4
Figure 5
Figure 6
Figure 7
Figure 8
Figure 9
Figure 10

Similar content being viewed by others

References

  • CT Ashley ST Warren (1995) ArticleTitleTrinucleotide repeat expansion and human disease Annu Rev Genet 29 703–728 Occurrence Handle10.1146/annurev.ge.29.120195.003415 Occurrence Handle1:CAS:528:DyaK28XlsFyq Occurrence Handle8825491

    Article  CAS  PubMed  Google Scholar 

  • WC Barker MO Dayhoff (1977) ArticleTitleEvolution of lipoproteins deduced from protein sequence data Comp Biochem Physiol B 57 309–315 Occurrence Handle10.1016/0305-0491(77)90060-8 Occurrence Handle1:CAS:528:DyaE2sXlsl2htL0%3D Occurrence Handle122556

    Article  CAS  PubMed  Google Scholar 

  • A Bateman L Coin R Durbin RD Finn V Hollich S Griffiths-Jones A Khanna M Marshall S Moxon ELL Sonnhammer DJ Studholme C Yeats SR Eddy (2004) ArticleTitleThe Pfam Protein Families Database Nucl Acids Res 32 D138–D141 Occurrence Handle10.1093/nar/gkh121 Occurrence Handle14681378

    Article  PubMed  Google Scholar 

  • HM Berman J Westbrook Z Feng G Gilliland TN Bhat H Weissig IN Shindyalov PE Bourne (2000) ArticleTitleThe Protein Data Bank Nucleic Acids Res 28 235–242 Occurrence Handle10.1093/nar/28.1.235 Occurrence Handle1:CAS:528:DC%2BD3cXhvVKjt7w%3D Occurrence Handle10592235

    Article  CAS  PubMed  Google Scholar 

  • CE Bonferroni (1936) ArticleTitleTeoria statistica delle classi e calcolo delle probabilita Pubbl R Ist Superiore Sci Econ Comm Firenze 8 3–62

    Google Scholar 

  • EU Canning (1988) ArticleTitleNuclear division and chromosome cycle in microsporidia Biosystems 21 333–340 Occurrence Handle10.1016/0303-2647(88)90030-5 Occurrence Handle1:STN:280:BieB1c7mtlM%3D Occurrence Handle3134965

    Article  CAS  PubMed  Google Scholar 

  • E Coward F Drablos (1998) ArticleTitleDetecting periodic patterns in biological sequences Bioinformatics 14 498–507 Occurrence Handle10.1093/bioinformatics/14.6.498 Occurrence Handle1:CAS:528:DyaK1cXmtFWltrc%3D Occurrence Handle9694988

    Article  CAS  PubMed  Google Scholar 

  • MT Cushion (2004) ArticleTitleComparative genomics of Pneumocystis carinii with other protists: Implications for life style J Eukaryotic Microbiol 51 30–37 Occurrence Handle1:CAS:528:DC%2BD2cXitleit70%3D

    CAS  Google Scholar 

  • CA Carpio-Munoz ParticleDel JC Carbajal (2002) ArticleTitleFolding pattern recognition in proteins using spectral analysis methods Genome Inform 13 163–172

    Google Scholar 

  • G Dover (2002) ArticleTitleMolecular drive Trends Genet 18 587–589 Occurrence Handle10.1016/S0168-9525(02)02789-0 Occurrence Handle12414190

    Article  PubMed  Google Scholar 

  • RV Eck MO Dayhoff (1966) ArticleTitleEvolution of the structure of ferridoxin based on living relics of primitive amino acid sequences Science 152 363–366 Occurrence Handle1:CAS:528:DyaF28XktFegtbo%3D

    CAS  Google Scholar 

  • D Eisenberg RM Weiss TC Terwilliger (1984) ArticleTitleThe hydrophobic moment detects periodicity in protein hydrophobicity Proc Natl Acad Sci USA 81 140–144 Occurrence Handle1:CAS:528:DyaL2cXhtFKlt7g%3D Occurrence Handle6582470

    CAS  PubMed  Google Scholar 

  • JE Galagan C Nusbaum A Roy MG Endrizzi P Macdonald W FitzHugh S Calvo R Engels S Smirnov D Atnoor A Brown N Alien J Naylor N Stange-Thomann K DeArellano R Johnson L Linton P McEwan K McKernan J Talamas A Tirrell W Ye A Zimmer RD Barber I Cann DE Graham DA Grahame AM Guss R Hedderich C Ingram-Smith HC Kuettner JA Krzycki JA Leigh W Li J Liu B Mukhopadhyay JN Reeve K Smith TA Springer LA Umayam O White RH White E Conway Macario Particlede JG Ferry KF Jarrell H Jing AJ Macario I Paulsen M Pritchett KR Sowers RV Swanson SH Zinder E Lander WW Metcalf B Birren (2002) ArticleTitleThe genome of M. acetivorans reveals extensive metabolic and physiological diversity Genome Res 12 532–542 Occurrence Handle1:CAS:528:DC%2BD38XivVemt74%3D Occurrence Handle11932238

    CAS  PubMed  Google Scholar 

  • D Gatherer NR McEwan (2003) ArticleTitleAnalysis of sequence periodicity in E. coli proteins: empirical investigation of the ‘duplication and divergence’ theory of protein evolution J Mol Evol 57 149–158 Occurrence Handle10.1007/s00239-002-2462-1 Occurrence Handle1:CAS:528:DC%2BD3sXmsFGrurg%3D Occurrence Handle14562959

    Article  CAS  PubMed  Google Scholar 

  • JW Golden HS Yoon (2003) ArticleTitleHeterocyst development in Anabaena Curr Opin Microbiol 6 557–563 Occurrence Handle10.1016/j.mib.2003.10.004 Occurrence Handle1:CAS:528:DC%2BD3sXps1yjsrw%3D Occurrence Handle14662350

    Article  CAS  PubMed  Google Scholar 

  • M Gruber AN Lupas (2003) ArticleTitleHistorical review: Another 50th anniversary - new periodicities in coiled coils Trends Biochem Sci 28 679–685 Occurrence Handle10.1016/j.tibs.2003.10.008 Occurrence Handle1:CAS:528:DC%2BD3sXpsVSksrY%3D Occurrence Handle14659700

    Article  CAS  PubMed  Google Scholar 

  • OC Ivanov CP Ivanov (1980) ArticleTitleSome evidence for the universality of structural periodicity in proteins J Mol Evol 16 47–68 Occurrence Handle1:CAS:528:DyaL3cXmtlehs74%3D Occurrence Handle7441779

    CAS  PubMed  Google Scholar 

  • MV Katti R Sami-Subbu PK Ranjekar VS Gupta (2000) ArticleTitleAmino acid repeat patterns in protein sequences: their diversity and structural-functional implications Prot Sci 9 1203–1209 Occurrence Handle1:CAS:528:DC%2BD3cXks1KqsLs%3D

    CAS  Google Scholar 

  • EV Korotkov MA Korotkova JS Tulko (1997) ArticleTitleLatent sequence periodicity of some oncogenes and DNA-binding protein genes Comp Appl Biosci 13 37–44 Occurrence Handle1:CAS:528:DyaK2sXis1antrc%3D Occurrence Handle9088707

    CAS  PubMed  Google Scholar 

  • MA Korotkova EV Korotkov VM Rundenko (1999) ArticleTitleLatent periodicity in protein sequences J Mol Model 5 103–115 Occurrence Handle10.1007/s008940050122 Occurrence Handle1:CAS:528:DyaK1MXks1Sisbc%3D

    Article  CAS  Google Scholar 

  • AA Laskin EV Korotkov MB Chaley NA Kudryashov (2003) ArticleTitleThe locally optimal method of cyclic alignment to reveal latent periodicities in genetic texts: the NAD-binding protein sites Mol Biol 37 561–570 Occurrence Handle10.1023/A:1025139427862 Occurrence Handle1:CAS:528:DC%2BD3sXmtFKksrs%3D

    Article  CAS  Google Scholar 

  • AD McLachlan M Stewart (1976) ArticleTitleThe 14-fold periodicity in alpha-tropomyosin and the interaction with actin J Mol Biol 103 271–298 Occurrence Handle10.1016/0022-2836(76)90313-2 Occurrence Handle1:CAS:528:DyaE28XktFGkur0%3D Occurrence Handle950663

    Article  CAS  PubMed  Google Scholar 

  • S Ohno (1984) ArticleTitleRepeats of base oligomers as the primordial coding sequences of the primeval earth and their vestiges in modern genes J Mol Evol 20 313–321 Occurrence Handle1:CAS:528:DyaL2cXmt1Gjs7g%3D Occurrence Handle6439885

    CAS  PubMed  Google Scholar 

  • S Ohno (1988) ArticleTitleCodon preference is but an illusion created by the construction principle of coding sequences Proc Natl Acad Sci USA 85 4378–4382 Occurrence Handle1:CAS:528:DyaL1cXks1yjtr4%3D Occurrence Handle3380799

    CAS  PubMed  Google Scholar 

  • N Pattabiraman K Namboodiri A Lowrey BP Gaber (1990) ArticleTitleNRL_\3D: a sequence-structure database derived from the Protein Data Bank (PDB) and searchable within the PIR environment Protein Sequences Data Anal 3 387–405 Occurrence Handle1:CAS:528:DyaK3MXmtFajsA%3D%3D

    CAS  Google Scholar 

  • GP Smith (1976) ArticleTitleEvolution of repeated DNA sequences by unequal crossover Science 191 528–535 Occurrence Handle1:CAS:528:DyaE28Xhs1Srurg%3D Occurrence Handle1251186

    CAS  PubMed  Google Scholar 

  • LE Stanfel (1996) ArticleTitleA new approach to clustering the amino acids J theoret Biol 183 195–205 Occurrence Handle10.1006/jtbi.1996.0213 Occurrence Handle1:CAS:528:DyaK2sXivVCmsg%3D%3D

    Article  CAS  Google Scholar 

  • EN Trifonov (1985) ArticleTitleSegmented structure of protein sequences and early evolution of genome by combinatorial fusion of DNA elements J Mol Evol 40 337–342 Occurrence Handle10.1007/BF00163239

    Article  Google Scholar 

  • M Vaara (1992) ArticleTitleEight bacterial proteins, including UDP-N-acetylglucosarnine acyltransferase (LpxA) and three other transferases of Escherichia coli, consist of a six-residue periodicity theme FEMS Microbiol Lett 76 249–254 Occurrence Handle10.1016/0378-1097(92)90344-N Occurrence Handle1:STN:280:ByyD2M7isFE%3D Occurrence Handle1427014

    Article  CAS  PubMed  Google Scholar 

  • SH White RE Jacobs (1993) ArticleTitleThe evolution of proteins from random amino acid sequences. I. Evidence from the lengthwise distribution of amino acids in modern protein sequences J Mol Evol 36 79–95 Occurrence Handle1:CAS:528:DyaK3sXnsFKlsQ%3D%3D Occurrence Handle8433379

    CAS  PubMed  Google Scholar 

  • M Ycas (1976) ArticleTitleOrigin of periodic proteins Fed Proc 35 2139–2140 Occurrence Handle1:CAS:528:DyaE28XltVGlsrc%3D Occurrence Handle947792

    CAS  PubMed  Google Scholar 

  • VS Zhurkin (1981) ArticleTitlePeriodicity in DNA primary structure is defined by secondary structure of the coded protein Nucleic Acids Res 9 1963–1971 Occurrence Handle1:CAS:528:DyaL3MXitVCjt74%3D Occurrence Handle7243595

    CAS  PubMed  Google Scholar 

  • JM Zimmerman N Eliezer R Simha (1968) ArticleTitleThe characterization of amino acid sequences in proteins by statistical methods J Theor Biol 21 170–201 Occurrence Handle10.1016/0022-5193(68)90069-6 Occurrence Handle1:CAS:528:DyaF1MXlsVSrsA%3D%3D Occurrence Handle5700434

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. MRC Virology Unit, Institute of Virology, University of Glasgow, Church Street, Glasgow, G11 5JR, UK

    Derek Gatherer

  2. Rowett Research Institute, Greenburn Road, Bucksburn, Aberdeen, AB21 9SB, UK

    Neil R. McEwan

Authors
  1. Derek Gatherer
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Neil R. McEwan
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Derek Gatherer.

Additional information

Reviewing Editor: Dr. John Oakeshott

Rights and permissions

Reprints and permissions

About this article

Cite this article

Gatherer, D., McEwan, N.R. Phylogenetic Differences in Content and Intensity of Periodic Proteins. J Mol Evol 60, 447–461 (2005). https://doi.org/10.1007/s00239-004-0189-2

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00239-004-0189-2

Keywords

Search

Navigation