Cite this paper:
YANG Feifei, XU Donghui, ZHUANG Yunyun, HUANG Yousong, YI Xiaoyan, CHEN Hongju, LIU Guangxing, ZHANG Huan. Characterization and analysis of ribosomal proteins in two marine calanoid copepods[J]. Journal of Oceanology and Limnology, 2016, 34(6): 1258-1268

Characterization and analysis of ribosomal proteins in two marine calanoid copepods

YANG Feifei1,2, XU Donghui2, ZHUANG Yunyun2, HUANG Yousong1, YI Xiaoyan1,2, CHEN Hongju1,2, LIU Guangxing1,2, ZHANG Huan1,2,3,
1 Key Laboratory of Marine Environment and Ecology(Ocean University of China), Ministry of Education, Qingdao 266100, China;
2 College of Environmental Science and Engineering, Ocean University of China, Qingdao 266100, China;
3 Department of Marine Sciences, University of Connecticut, Groton, Connecticut 06340, USA
Abstract:
Copepods are among the most abundant and successful metazoans in the marine ecosystem. However, genomic resources related to fundamental cellular processes are still limited in this particular group of crustaceans. Ribosomal proteins are the building blocks of ribosomes, the primary site for protein synthesis. In this study, we characterized and analyzed the cDNAs of cytoplasmic ribosomal proteins (cRPs) of two calanoid copepods, Pseudodiaptomus poplesia and Acartia pacifica. We obtained 79 cRP cDNAs from P. poplesia and 67 from A. pacifica by cDNA library construction/sequencing and rapid amplification of cDNA ends. Analysis of the nucleic acid composition showed that the copepod cRP-encoding genes had higher GC content in the protein-coding regions (CDSs) than in the untranslated regions (UTRs), and single nucleotide repeats (>3 repeats) were common, with "A" repeats being the most frequent, especially in the CDSs. The 3'-UTRs of the cRP genes were significantly longer than the 5'-UTRs. Codon usage analysis showed that the third positions of the codons were dominated by C or G. The deduced amino acid sequences of the cRPs contained high proportions of positively charged residues and had high pI values. This is the first report of a complete set of cRP-encoding genes from copepods. Our results shed light on the characteristics of cRPs in copepods, and provide fundamental data for further studies of protein synthesis in copepods. The copepod cRP information revealed in this study indicates that additional comparisons and analysis should be performed on different taxonomic categories such as orders and families.
Key words:    amino acid composition|codon usage|copepod|nucleotide composition|ribosomal protein   
Received: 2015-04-20   Revised: 2015-07-20
Tools
PDF (510 KB) Free
Print this page
Add to favorites
Email this article to others
Authors
Articles by YANG Feifei
Articles by XU Donghui
Articles by ZHUANG Yunyun
Articles by HUANG Yousong
Articles by YI Xiaoyan
Articles by CHEN Hongju
Articles by LIU Guangxing
Articles by ZHANG Huan
References:
Barreto F S, Burton R S. 2013. Evidence for compensatory evolution of ribosomal proteins in response to rapid divergence of mitochondrial rRNA. Mol. Biol. Evol., 30(2):310-314.
Blanco-Bercial L, Bradford-Grieve J, Bucklin A. 2011.Molecular phylogeny of the Calanoida (Crustacea:Copepoda). Mol. Phylogenet. Evol., 59(1):103-113.
Botzman M, Margalit H. 2011. Variation in global codon usage bias among prokaryotic organisms is associated with their lifestyles. Genome Biol., 12(10):R109.
Brodersen D E, Clemons Jr W M, Carter A P, Wimberly B T, Ramakrishnan V. 2002. Crystal structure of the 30S ribosomal subunit from Thermus thermophilus:structure of the proteins and their interactions with 16S RNA. J.Mol. Biol., 316(3):725-768.
Bulmer M. 1990. The effect of context on synonymous codon usage in genes with low codon usage bias. Nucl. Acids Res., 18(10):2 869-2 873.
Burton B, Zimmermann M T, Jernigan R L, Wang Y M. 2012.A computational investigation on the connection between dynamics properties of ribosomal proteins and ribosome assembly. PLoS Comput. Biol., 8(5):e1002530, http://dx.doi.org/10.1371/journal.pcbi.1002530.
Causton H C, Ren B, Koh S S, Harbison C T, Kanin E, Jennings E G, Lee T I, True H L, Lander E S, Young R A. 2001.Remodeling of yeast genome expression in response to environmental changes. Mol. Biol. Cell, 12(2):323-337.
Cutter A D, Payseur B A, Salcedo T, Estes A M, Good J M, Wood E, Hartl T, Maughan H, Strempel J, Wang B M, Bryan A C, Dellos M. 2003. Molecular correlates of genes exhibiting RNAi phenotypes in Caenorhabditis elegans.Genome Res., 13(12):2 651-2 657.
Grocock R J, Sharp P M. 2002. Synonymous codon usage in Pseudomonas aeruginosa PA01. Gene, 289(1-2):131-139.
Gupta S K, Bhattacharyya T K, Ghosh T C. 2004. Synonymous codon usage in Lactococcus lactis:mutational bias versus translational selection. J. Biomol. Struct. Dyn., 21(4):527-535.
Harris J K, Kelley S T, Spiegelman G B, Pace N R. 2003. The genetic core of the universal ancestor. Genome Res., 13(3):407-412.
Heitzer M, Eckert A, Fuhrmann M, Griesbeck C. 2007.Influence of codon bias on the expression of foreign genes in microalgae. Adv. Exp. Med. Biol., 616, 46-53.
Humes A G. 1994. How many copepods? Hydrobiologia, 292(1):1-7.
Ikemura T. 1981. Correlation between abundance of Escherichia coli transfer RNAs and the occurrence of the respective codons in its protein genes:a proposal for a synonymous codon choice that is optimal for the E. coli translational system. J. Mol. Biol., 151(3):389-409.
Ishii K, Washio T, Uechi T, Yoshihama M, Kenmochi N, Tomita M. 2006. Characteristics and clustering of human ribosomal protein genes. BMC Genomics, 7(1):37.
Kiørboe T. 2011. What makes pelagic copepods so successful?J. Plankton Res., 33(5):677-685.
Kober K M, Pogson G H. 2013. Genome-wide patterns of codon bias are shaped by natural selection in the purple sea urchin, Strongylocentrotus purpuratus. G3, 3(7):1 069-1 083.
Kozak M. 1986. Point mutations define a sequence flanking the AUG initiator codon that modulates translation by eukaryotic ribosomes. Cell, 44(2):283-292.
Kudla G, Murray A W, Tollervey D, Plotkin J B. 2009. Codingsequence determinants of gene expression in Escherichia coli. Science, 324(5924):255-258.
Lecompte O, Ripp R, Thierry J C, Moras D, Poch O. 2002.Comparative analysis of ribosomal proteins in complete genomes:an example of reductive evolution at the domain scale. Nucleic Acids Res., 30(24):5 382-5 390.
Lindström M S. 2009. Emerging functions of ribosomal proteins in gene-specific transcription and translation.Biochem. Bioph. Res. Co., 379(2):167-170.
Liu D L, Brockman J M, Dass B, Hutchins L N, Singh P, McCarrey J R, MacDonald C C, Graber J H. 2007.Systematic variation in mRNA 3'-processing signals during mouse spermatogenesis. Nucleic Acids Res., 35(1):234-246.
Lott B B, Wang Y M, Nakazato T. 2013. A comparative study of ribosomal proteins:linkage between amino acid distribution and ribosomal assembly. BMC Biophys., 6(1):13.
Marygold S J, Roote J, Reuter G, Lambertsson A, Ashburner M, Millburn G H, Harrison P M, Yu Z, Kenmochi N, Kaufman T C, Leevers S J, Cook K R. 2007. The ribosomal protein genes and Minute loci of Drosophila melanogaster. Genome Biol., 8(10):R216.
Miller C B, Wheeler P. 2004. Biological Oceanography.Blackwell Publishing, Oxford, UK. p.111-128.
Peden J F. 1999. Analysis of Codon Usage. University of Nottingham, UK.
Powers T, Walter P. 1999. Regulation of ribosome biogenesis by the rapamycin-sensitive TOR-signaling pathway in Saccharomyces cerevisiae. Mol. Biol. Cell, 10(4):987-1 000.
Rhee J S, Raisuddin S, Lee K W, Seo J S, Ki J S, Kim I C, Park H G, Lee J S. 2009. Heat shock protein (Hsp) gene responses of the intertidal copepod Tigriopus japonicus to environmental toxicants. Comp. Biochem. Phys. C., 149(1):104-112.
Rispe C, Legeai F, Gauthier J P, Tagu D. 2007. Strong heterogeneity in nucleotidic composition and codon bias in the pea aphid (Acyrthosiphon pisum) shown by ESTbased coding genome reconstruction. J. Mol. Evol., 65(4):413-424.
RoyChoudhury S, Mukherjee D. 2010. A detailed comparative analysis on the overall codon usage pattern in herpesviruses. Virus Res., 148(1-2):31-43.
Sen G, Sur S, Bose D, Mondal U, Furnholm T, Bothra A, Tisa L, Sen A. 2007. Analysis of codon usage patterns and predicted highly expressed genes for six phytopathogenic Xanthomonas genomes shows a high degree of conservation. In Silico Boil., 7(4-5):547-558.
Sharp P M, Li W H. 1986. An evolutionary perspective on synonymous codon usage in unicellular organisms. J.Mol. Evol., 24(1-2):28-38.
Sharp P M, Li W H. 1987. The codon adaptation index-a measure of directional synonymous codon usage bias, and its potential applications. Nucleic Acids Res., 15(3):1 281-1 295.
Sørensen H P, Mortensen K K. 2005. Advanced genetic strategies for recombinant protein expression in Escherichia coli. J. Biotechnol., 115(2):113-128.
Sur S, Bhattacharya M, Bothra A K, Tisa L S, Sen A. 2008.Bioinformatic analysis of codon usage patterns in a free living diazotroph, Azotobacter vinelandii. Biotechnology, 7(2):242-249.
Verdoes J C, van Ooyen A J J. 2000. Codon usage in Xanthophyllomyces dendrorhous (formerly Phaffia rhodozyma). Biotechnol. Lett., 22(1):9-13.
Warner J R, McIntosh K B. 2009. How common are extraribosomal functions of ribosomal proteins? Mol.Cell, 34(1):3-11.
Warner J R. 1999. The economics of ribosome biosynthesis in yeast. Trends Biochem. Sci., 24(11):437-440.
Wilson D N, Cate J H D. 2012. The structure and function of the eukaryotic ribosome. Cold Spring Harb. Perspect.Biol., 4(5):a011536.
Wright F. 1990. The ‘effective number of codons’ used in a gene. Gene, 87(1):23-29.
Wu G, Culley D E, Zhang W W. 2005. Predicted highly expressed genes in the genomes of Streptomyces coelicolor and Streptomyces avermitilis and the implications for their metabolism. Microbiology, 151(7):2 175-2 187.
Xu C, Dong J, Tong C F, Gong X D, Wen Q, Zhuge Q. 2013.Analysis of synonymous codon usage patterns in seven different citrus species. Evol. Bioinform., 9:215-228.
Yang F F, Xu D H, Zhuang Y Y, Yi X Y, Huang Y S, Chen H J, Lin S J, Campbell D A, Sturm N R, Liu G X, Zhang H. 2015. Spliced leader RNA trans-splicing discovered in copepods. Sci. Rep.-UK, 5:17 411, http://dx.doi.org/10.1038/srep17411.
Zhang H, Finiguerra M, Dam H G, Huang Y S, Xu D H, Liu G X, Lin S J. 2013. An improved method for achieving highquality RNA for copepod transcriptomic studies. J. Exp.Mar. Biol. Ecol., 446:57-66.
Zhang H, Hou Y B, Miranda L, Campbell D A, Sturm N R, Gaasterland T, Lin S J. 2007. Spliced leader RNA transsplicing in dinoflagellates. Proc. Natl. Acad. Sci. USA, 104(11):4 618-4 623.
Copyright © Haiyang Xuebao