Abstract
The codon usage patterns of rhizobia have received increasing attention. However, little information is available regarding the conserved features of the codon usage patterns in a typical rhizobial genus. The codon usage patterns of six completely sequenced strains belonging to the genus Rhizobium were analysed as model rhizobia in the present study. The relative neutrality plot showed that selection pressure played a role in codon usage in the genus Rhizobium. Spearman’s rank correlation analysis combined with correspondence analysis (COA) showed that the codon adaptation index and the effective number of codons (ENC) had strong correlation with the first axis of the COA, which indicated the important role of gene expression level and the ENC in the codon usage patterns in this genus. The relative synonymous codon usage of Cys codons had the strongest correlation with the second axis of the COA. Accordingly, the usage of Cys codons was another important factor that shaped the codon usage patterns in Rhizobium genomes and was a conserved feature of the genus. Moreover, the comparison of codon usage between highly and lowly expressed genes showed that 20 unique preferred codons were shared among Rhizobium genomes, revealing another conserved feature of the genus. This is the first report of the codon usage patterns in the genus Rhizobium.
Similar content being viewed by others
References
Das S, Pan A, Paul S, Dutta C (2005) Comparative analyses of codon and amino acid usage in symbiotic island and core genome in nitrogen-fixing symbiotic bacterium Bradyrhizobium japonicum. J Biomol Struct Dyn 23(2):221–232
González V, Santamaría RI, Bustos P, Hernández-González I, Medrano-Soto A, Moreno-Hagelsieb G, Janga SC, Ramírez MA, Jiménez-Jacinto V, Collado-Vides J, Dávila G (2006) The partitioned Rhizobium etli genome: genetic and metabolic redundancy in seven interacting replicons. P Natl Acad Sci USA 103(10):3834–3839
Hershberg R, Petrov DA (2009) General rules for optimal codon choice. PLoS Genet 5(7):e1000556
Iriarte A, Baraibar JD, Romero H, Musto H (2011) Selected codon usage bias in members of the class Mollicutes. Gene 473(2):110–118
Juminaga D, Baidoo EEK, Redding-Johanson AM, Batth TS, Burd H, Mukhopadhyay A, Petzold CJ, Keasling JD (2012) Modular engineering of l-tyrosine production in Escherichia coli. Appl Environ Microb 78(1):89–98
Jung SK, McDonald K (2011) Visual gene developer: a fully programmable bioinformatics software for synthetic gene optimization. BMC Bioinform 12(1):340
Kong W, Kong J, Hu S, Lu W, Wang K, Ji M (2011) Enhanced expression of PCV2 capsid protein in Escherichia coli and Lactococcus lactis by codon optimization. World J Microbiol Biotechnol 27(3):651–657
Lozano L, Hernández-González I, Bustos P, Santamaría RI, Souza V, Young JPW, Dávila G, González V (2010) Evolutionary dynamics of insertion sequences in relation to the evolutionary histories of the chromosome and symbiotic plasmid genes of Rhizobium etli populations. Appl Environ Microb 76(19):6504–6513
Lynn DJ, Singer GAC, Hickey DA (2002) Synonymous codon usage is subject to selection in thermophilic bacteria. Nucleic Acids Res 30(19):4272–4277
Nayak KC (2012) Comparative study on factors influencing the codon and amino acid usage in Lactobacillus sakei 23 K and 13 other lactobacilli. Mol Biol Rep 39(1):535–545
Novembre JA (2002) Accounting for background nucleotide composition when measuring codon usage bias. Mol Biol Evol 19(8):1390–1394
Ormeño-Orrillo E, Rogel-Hernández M, Lloret L, López-López A, Martínez J, Barois I, Martínez-Romero E (2012) Change in land use alters the diversity and composition of Bradyrhizobium communities and led to the introduction of Rhizobium into the tropical rain forest of Los Tuxtlas (Mexico). Microb Ecol 63(4):822–834
Peixoto L, Zavala A, Romero H, Musto H (2003) The strength of translational selection for codon usage varies in the three replicons of Sinorhizobium meliloti. Gene 320:109–116
Rao Y, Wu G, Wang Z, Chai X, Nie Q, Zhang X (2011) Mutation bias is the driving force of codon usage in the Gallus gallus genome. DNA Res 18(6):499–512
Reeve W, Hara GO, Chain P, Ardley J, Bräu L, Nandesena K, Tiwari R, Copeland A, Nolan M, Han C (2010a) Complete genome sequence of Rhizobium leguminosarum bv. trifolii strain WSM1325, an effective microsymbiont of annual Mediterranean clovers. Stand Genomic Sci 2(3):347–356
Reeve W, Hara GO, Chain P, Ardley J, Bräu L, Nandesena K, Tiwari R, Malfatti S, Kiss H, Lapidus A (2010b) Complete genome sequence of Rhizobium leguminosarum bv trifolii strain WSM2304, an effective microsymbiont of the South American clover Trifolium polymorphum. Stand Genomic Sci 2(1):66–76
Sablok G, Nayak KC, Vazquez F, Tatarinova TV (2011) Synonymous codon usage, GC 3, and evolutionary patterns across plastomes of three pooid model species: emerging grass genome models for monocots. Mol Biotechnol 49(2):116–128
Sanjukta R, Farooqi MS, Sharma N, Rai A, Mishra DC, Singh DP (2012) Trends in the codon usage patterns of Chromohalobacter salexigens genes. Bioinformation 8(22):1087–1095
Sen A, Sur S, Bothra AK, Benson DR, Normand P, Tisa LS (2008) The implication of life style on codon usage patterns and predicted highly expressed genes for three Frankia genomes. Anton Leeuw Int JG 93(4):335–346
Sharp PM, Li WH (1986) Codon usage in regulatory genes in Escherichia coli does not reflect selection for ‘rare’codons. Nucleic Acids Res 14(19):7737–7749
Slater SC, Goldman BS, Goodner B, Setubal JC, Farrand SK, Nester EW, Burr TJ, Banta L, Dickerman AW, Paulsen I (2009) Genome sequences of three Agrobacterium biovars help elucidate the evolution of multichromosome genomes in bacteria. J Bacteriol 191(8):2501–2511
Sueoka N (1988) Directional mutation pressure and neutral molecular evolution. P Natl Acad Sci USA 85(8):2653–2657
Sur S, Bhattacharya M, Bothra AK, Tisa LS, Sen A (2008) Bioinformatic analysis of codon usage patterns in a free-living diazotroph, Azotobacter vinelandii. Biotechnology 7(2):242–249
Villaseñor T, Brom S, Dávalos A, Lozano L, Romero D, Los Santos AG (2011) Housekeeping genes essential for pantothenate biosynthesis are plasmid-encoded in Rhizobium etli and Rhizobium leguminosarum. BMC Microbiol 11(1):66
Willenbrock H, Friis C, Juncker AS, Ussery DW (2006) An environmental signature for 323 microbial genomes based on codon adaptation indices. Genome Biol 7(12):R114
Wright F (1990) The 'effective number of codons' used in a gene. Gene 87:23–29
Young JPW, Crossman LC, Johnston AWB, Thomson NR, Ghazoui ZF, Hull KH, Wexler M, Curson ARJ, Todd JD, Poole PS (2006) The genome of Rhizobium leguminosarum has recognizable core and accessory components. Genome Biol 7(4):R34
Yu T, Li J, Yang Y, Qi L, Chen B, Zhao F, Bao Q, Wu J (2012) Codon usage patterns and adaptive evolution of marine unicellular cyanobacteria Synechococcus and Prochlorococcus. Mol Phylogenet Evol 62(1):206–213
Zavala A, Naya H, Romero H, Musto H (2002) Trends in codon and amino acid usage in Thermotoga maritima. J Mol Evol 54(5):563–568
Zhao S, Zhang Q, Chen Z, Zhong J (2008) The factors dictating the codon usage variation among the genes in the genome of Burkholderia pseudomallei. World J Microbiol Biotechnol 24(8):1585–1592
Acknowledgments
This work was supported by the science and technology project from China National Offshore Oil Corporation (No. CNOOC-KJ 125 ZDXM 00 000 00 NFCY 2011-04).
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Wang, X., Wu, L., Zhou, P. et al. Analysis of synonymous codon usage patterns in the genus Rhizobium . World J Microbiol Biotechnol 29, 2015–2024 (2013). https://doi.org/10.1007/s11274-013-1364-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11274-013-1364-7