Skip to main content
SpringerLink
Log in

The implication of life style on codon usage patterns and predicted highly expressed genes for three Frankia genomes

  • Original Paper
  • Published:
Antonie van Leeuwenhoek Aims and scope Submit manuscript

Abstract

Frankia are nitrogen-fixing actinomycetes that form a symbiotic association with over 200 species of woody dicotyledonous plants. Recently, three Frankia genomes were completely sequenced. In this study, the synonymous codon usage patterns of three Frankia genomes (strains CcI3, ACN14a, and EAN1pec) were determined and compared to each other and to other actinobacteria. As expected for a high G+C organism, codon usage by Frankia was highly biased, but differences were observed among the three strains. Using the codon adaptation index (CAI) as a numerical estimator of gene expression level, highly expressed genes in Frankia were predicted with ribosomal protein genes as a reference. The analysis of the predicted highly expressed genes showed that Frankia strain CcI3 had a different profile from the other two strains. Strain CcI3 had fewer predicted highly expressed genes in several COG categories including lipid transport and metabolism, secondary metabolites biosynthesis, inorganic ion transport and metabolism, and general function prediction only than Frankia strains EAN1pec and ACN14a. Interestingly, Frankia EAN1pec had more predicted highly expressed genes in transcription and signal transduction mechanisms than the other two strains. These differences were not just a reflection in total gene numbers, but also based on percentage of genes within a category. These results support the hypothesis that strain CcI3 is becoming a symbiotic specialist and the other two facultative symbiotic strains are maintaining their capacity to exist as free-living soil dwellers.

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Abbreviations

COG:

Clusters of orthologous groups of proteins

CDS:

Protein coding sequences

CAI:

Codon adaptation index

References

  • Banerjee T, Basak S, Gupta SK, Ghosh TC (2004) Evolutionary forces in shaping codon and amino acid usages in Blochmannia floridanus. J Biomol Struct Dyn 22:13–23

    PubMed  CAS  Google Scholar 

  • Benson DR, Dawson JO (2007) Recent advances in the biogeography and genecology of symbiotic Frankia and its host plants. Physiol Plant 130:318–330

    Article  CAS  Google Scholar 

  • Benson DR, Silvester WB (1993) Biology of Frankia strains, actinomycete symbionts of actinorhizal plants. Microbiol Rev 57:293–319

    PubMed  CAS  Google Scholar 

  • Bentley SD, Chater KF, Cerdeno-Tarraga AM, Challis GL, Thomson NR, James KD, Harris DE, Quail MA, Kieser H, Harper D, Bateman A, Brown S, Chandra G, Chen CW, Collins M, Cronin A, Fraser A, Goble A, Hidalgo J, Hornsby T, Howarth S, Huang CH, Kieser T, Larke L, Murphy L, Oliver K, O’Neil S, Rabbinowitsch E, Rajandream MA, Rutherford K, Rutter S, Seeger K, Saunders D, Sharp S, Squares R, Squares S, Taylor K, Warren T, Wietzorrek A, Woodward J, Barrell BG, Parkhill J, Hopwood DA (2002) Complete genome sequence of the model actinomycete Streptomyces coelicolor A3(2). Nature 417:141–147

    Article  PubMed  Google Scholar 

  • Cameron J, Aguadé M (1998) An evaluation of measures of synonymous codon usage bias. J Mol Evol 47:268–274

    Article  Google Scholar 

  • Dos Reis M, Wernisch L, Savva R (2003) Unexpected correlations between gene expression and codon usage bias from microarray data for the whole Escherichia coli K-12 genome. Nucleic Acids Res 31:6976–6985

    Article  PubMed  CAS  Google Scholar 

  • Ghosh TC, Gupta SK, Majumdar S (2000) Studies on codon usage in Entamoeba histolytica. Int J Parasitol 30:715–722

    Article  PubMed  CAS  Google Scholar 

  • Grantham R, Gautier C, Gouy M, Jacobzone M, Mercier R (1981) Codon catalog usage is a genome strategy modulated for gene expressivity. Nucleic Acids Res 9:r43–r74

    Article  PubMed  CAS  Google Scholar 

  • Greenacre MJ (1984) Theory and applications of correspondence analysis. Academic Press, London

    Google Scholar 

  • Huss-Danell K (1997) Actinorhizal symbioses and their N2 fixation. Tansley Review No. 93. New Phytol 136:375–405

    Article  CAS  Google Scholar 

  • Ikemura T (1981) Correlation between the abundance of Escherichia coli transfer RNAs and the occurrence of the respective codons in its protein genes. J Mol Biol 146:1–21

    Article  PubMed  CAS  Google Scholar 

  • Ikemura T (1985) Codon usage and t-RNA content in unicellular and multicellular organisms. Mol Biol Evol 2:13–34

    PubMed  CAS  Google Scholar 

  • Jansen R, Bussemaker HJ, Gerstein M (2003) Revisiting the codon adaptation index from a whole-genome perspective: analyzing the relationship between gene expression and codon occurrence in yeast using a variety of models. Nucleic Acids Res 31:2242–2251

    Article  PubMed  CAS  Google Scholar 

  • Karlin S, Mrazek J (2000) Predicted highly expressed genes of diverse prokaryotic genomes. J Bacteriol 182:5238–5250

    Article  PubMed  CAS  Google Scholar 

  • Karlin S, Mrazek J, Campbell A, Kaiser D (2001) Characterizations of highly expressed genes of four fast-growing bacteria. J Bacteriol 183:5025–5040

    Article  PubMed  CAS  Google Scholar 

  • Knight RD, Freeland SJ, Landweber LF (2001) A simple model based on mutation and selection explains trends in codon and amino-acid usage and GC composition within and across genomes. Genome Biol 2(4):research0010.1–0010.13; doi: 10.1186/gb-2001-2-4- research0010

  • Lafay B, Atherton JC, Sharp PM (2000) Absence of translationally selected synonymous codon usage bias in Helicobacter pylori. Microbiology 146:851–860

    PubMed  CAS  Google Scholar 

  • Markowitz VM, Ivanova N, Palaniappan K, Szeto E, Korzeniewski F, Lykidis A, Anderson I, Mavrommatis K, Kunin V, Garcia Martin H, Dubchak I, Hugenholtz P, Kyrpides NC (2006) An experimental metagenome data management and analysis system. Bioinformatics 22:e359–e367

    Article  PubMed  CAS  Google Scholar 

  • Martin-Galiano AJ, Wells JM, de la Campa AG (2004) Relationship between codon biased genes, microarray expression values and physiological characteristics of Streptococcus pneumoniae. Microbiology 150:2313–2325

    Article  PubMed  CAS  Google Scholar 

  • Normand P, Lapierre P, Tisa LS, Gogarten JP, Alloisio N, Bagnarol E, Bassi CA, Berry AM, Bickhart DM, Choisne N, Couloux A, Cournoyer B, Cruveiller S, Daubin V, Demange N, Francino MP, Goltsman E, Huang Y, Kopp OR, Labarre L, Lapidus A, Lavire C, Marechal J, Martinez M, Mastronunzio JE, Mullin BC, Niemann J, Tania PP, Zoe Rouy R, Schenowitz C, Sellstedt A, Tavares F, Tomkins JP, Vallenet D, Valverde C, Wall LG, Wang Y, Medigue SC, Benson DR (2007) Genome characteristics of facultative symbiotic Frankia sp. strains reflect host range and host plant biogeography. Genome Res 7:7–15

    Google Scholar 

  • Peden J (1999) Analysis of codon usage. PhD thesis, The University of Nottingham, UK

  • Sellstedt A (1995) Specificity and effectivity in nodulation by Frankia on southern hemisphere actinorhiza. FEMS Microbiol Lett 125:231–236

    Article  PubMed  CAS  Google Scholar 

  • Sharp PM, Li WH (1986) An evolutionary perspective on synonymous codon usage in unicellular organisms. J Mol Evol 24:28–38

    Article  PubMed  CAS  Google Scholar 

  • Sharp PM, Li WH (1987) The codon adaptation index – a measure of directional synonymous codon usage bias, and its potential applications. Nucleic Acids Res 15:1281–1295

    Article  PubMed  CAS  Google Scholar 

  • Simonet P, Navarro E, Rouvier C, Reddell P, Zimpfer J, Dommergues Y, Bardin R, Combarro P, Hamelin J, Domenach AM, Gourbiere F, Prin Y, Dawson J, Normand P (1999) Co-evolution between Frankia populations and host plants in the family Casuarinaceae and consequent patterns of global dispersal. Environ Microbiol 1:525–533

    Article  PubMed  CAS  Google Scholar 

  • Sur S, Sen A, Bothra AK (2006) Codon usage profiling and analysis of intergenic association of Frankia EuIK1 nif genes. Ind J Microbiol 46:363–369

    CAS  Google Scholar 

  • Wall LG (2000) The actinorhizal symbiosis. J Plant Growth Regul 19:167–182

    PubMed  CAS  Google Scholar 

  • Wright F (1990) The effective number of codons used in a gene. Gene 87:23–29

    Article  PubMed  CAS  Google Scholar 

  • Wu G, Culley DE, Zhang W (2005a) Predicted highly expressed genes in the genomes of Streptomyces coelicolor and Streptomyces avermitilis and the implications for their metabolism. Microbiology 151:2175–2187

    Article  PubMed  CAS  Google Scholar 

  • Wu G, Nie L, Zhang W (2005b) Predicted highly expressed genes in Nocardia farcinica and the implication for its primary metabolism and nocardial virulence. Antonie Van Leeuwenhoek 89:135–146

    Article  Google Scholar 

  • Zimpfer JF, Smyth CA, Dawson JO (1997) The capacity of Jamaican mine spoils, agricultural and forest soils to nodulate Myrica cerifera, Leucaena leucocephala and Casuarina cunninghamiana. Physiol Plant 99:664–672

    Article  CAS  Google Scholar 

Download references

Acknowledgements

The authors are grateful to the Department of Biotechnology, Government of India, for providing financial help in setting up Bioinformatics Infrastructural Facility in the Department of Botany, University of North Bengal. Arnab Sen acknowledges DBT for providing an Overseas Fellowship. This investigation was supported in part by USA NSF EF-0333177, DBT Overseas Associateship (India), and by the College of Life Sciences and Agriculture, University of New Hampshire, Durham.

Author information

Authors and Affiliations

  1. Department of Microbiology, University of New Hampshire, 46 College Rd., Durham, NH, 03824-2617, USA

    Arnab Sen & Louis S. Tisa

  2. Department of Botany, University of North Bengal, Siliguri, 734013, India

    Arnab Sen & Saubashya Sur

  3. Raiganj University College, Raiganj, India

    Asim K. Bothra

  4. Department of Cellular and Molecular Biology, University of Connecticut, Storrs, CT, 06279, USA

    David R. Benson

  5. Ecologie Microbienne, UMR CNRS 5557, Université Lyon I, Villeurbanne Cedex, 69622, France

    Philippe Normand

Authors
  1. Arnab Sen
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Saubashya Sur
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Asim K. Bothra
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. David R. Benson
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Philippe Normand
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Louis S. Tisa
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Louis S. Tisa.

Electronic supplementary material

Below is the link to the electronic supplementary material.

(XLS 109 kb)

(XLS 72 kb)

(XLS 121 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Sen, A., Sur, S., Bothra, A.K. et al. The implication of life style on codon usage patterns and predicted highly expressed genes for three Frankia genomes. Antonie van Leeuwenhoek 93, 335–346 (2008). https://doi.org/10.1007/s10482-007-9211-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10482-007-9211-1

Keywords

Search

Navigation