Diversity, mobility, and structural and functional evolution of group II introns carrying an unusual 3' extension

BMC Research Notes

Anne-Brit Kolstø¹  Fredrik B Stabell³  Nicolas J Tourasse² 

[1] Laboratory for Microbial Dynamics (LaMDa), Department of Pharmaceutical Biosciences, University of Oslo, Oslo, Norway;Institut de Biologie Physico-Chimique, UMR CNRS 7141, Université Pierre et Marie Curie, 13 rue Pierre et Marie Curie, 75005 Paris, France;GeoKnowledge AS, Oslo, Norway

关键词: Mobility;    Plasmid;    pXO1-42;    Evolution;    Unusual extension;    Group II intron;   

Others  :  1166836
DOI  :  10.1186/1756-0500-4-564

 received in 2011-09-10, accepted in 2011-12-28,  发布年份 2011

【 摘 要 】

Background

Group II introns are widespread genetic elements endowed with a dual functionality. They are catalytic RNAs (ribozymes) that are able of self-splicing and they are also mobile retroelements that can invade genomic DNA. The group II intron RNA secondary structure is typically made up of six domains. However, a number of unusual group II introns carrying a unique extension of 53-56 nucleotides at the 3' end have been identified previously in bacteria of the Bacillus cereus group.

Methods

In the present study, we conducted combined sequence comparisons and phylogenetic analyses of introns, host gene, plasmid and chromosome of host strains in order to gain insights into mobility, dispersal, and evolution of the unusual introns and their extension. We also performed in vitro mutational and kinetic experiments to investigate possible functional features related to the extension.

Results

We report the identification of novel copies of group II introns carrying a 3' extension including the first two copies in bacteria not belonging to the B. cereus group, Bacillus pseudofirmus OF4 and Bacillus sp. 2_A_57_CT2, an uncharacterized species phylogenetically close to B. firmus. Interestingly, the B. pseudofirmus intron has a longer extension of 70 bases. From sequence comparisons and phylogenetic analyses, several possible separate events of mobility involving the atypical introns could be identified, including both retrohoming and retrotransposition events. In addition, identical extensions were found in introns that otherwise exhibit little sequence conservation in the rest of their structures, with the exception of the conserved and catalytically critical domains V and VI, suggesting either separate acquisition of the extra segment by different group II introns or a strong selection pressure acting on the extension. Furthermore, we show by in vitro splicing experiments that the 3' extension affects the splicing properties differently in introns belonging to separate evolutionary branches.

Conclusions

Altogether this study provides additional insights into the structural and functional evolution of unusual introns harboring a 3' extension and lends further evidence that these introns are mobile with their extension.

【 授权许可】

   
2011 Tourasse et al; licensee BioMed Central Ltd

【 图 表 】

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【 参考文献 】

• [1]Lambowitz AM, Zimmerly S: Mobile group II introns. Annu Rev Genet 2004, 38:1-35.
• [2]Pyle AM, Lambowitz AM: Group II introns: ribozymes that splice RNA and invade DNA. In The RNA world. third edition. Edited by Gesteland RF, Cech TR, Atkins JF. Cold Spring Harbor, N.Y.: Cold Spring Harbor Laboratory Press; 2006:469-505. vol. Cold Spring Harbor monograph series 43
• [3]Robart AR, Zimmerly S: Group II intron retroelements: function and diversity. Cytogenet Genome Res 2005, 110(1-4):589-597.
• [4]Toro N, Jimenez-Zurdo JI, Garcia-Rodriguez FM: Bacterial group II introns: not just splicing. FEMS Microbiol Rev 2007, 31(3):342-358.
• [5]Lehmann K, Schmidt U: Group II introns: structure and catalytic versatility of large natural ribozymes. Crit Rev Biochem Mol Biol 2003, 38(3):249-303.
• [6]Chin K, Pyle AM: Branch-point attack in group II introns is a highly reversible transesterification, providing a potential proofreading mechanism for 5'-splice site selection. RNA 1995, 1(4):391-406.
• [7]Chu VT, Liu Q, Podar M, Perlman PS, Pyle AM: More than one way to splice an RNA: branching without a bulge and splicing without branching in group II introns. RNA 1998, 4(10):1186-1202.
• [8]Daniels DL, Michels WJ Jr, Pyle AM: Two competing pathways for self-splicing by group II introns: a quantitative analysis of in vitro reaction rates and products. J Mol Biol 1996, 256(1):31-49.
• [9]Jarrell KA, Peebles CL, Dietrich RC, Romiti SL, Perlman PS: Group II intron self-splicing. Alternative reaction conditions yield novel products. J Biol Chem 1988, 263(7):3432-3439.
• [10]Peebles CL, Benatan EJ, Jarrell KA, Perlman PS: Group II intron self-splicing: development of alternative reaction conditions and identification of a predicted intermediate. Cold Spring Harb Symp Quant Biol 1987, 52:223-232.
• [11]Dai L, Zimmerly S: Compilation and analysis of group II intron insertions in bacterial genomes: evidence for retroelement behavior. Nucleic Acids Res 2002, 30(5):1091-1102.
• [12]Klein JR, Dunny GM: Bacterial group II introns and their association with mobile genetic elements. Front Biosci 2002, 7:d1843-d1856.
• [13]Tourasse NJ, Kolstø AB: Survey of group I and group II introns in 29 sequenced genomes of the Bacillus cereus group: insights into their spread and evolution. Nucleic Acids Res 2008, 36(14):4529-4548.
• [14]Dai L, Chai D, Gu SQ, Gabel J, Noskov SY, Blocker FJ, Lambowitz AM, Zimmerly S: A three-dimensional model of a group II intron RNA and its interaction with the intron-encoded reverse transcriptase. Mol Cell 2008, 30:1-14.
• [15]Toor N, Keating KS, Taylor SD, Pyle AM: Crystal structure of a self-spliced group II intron. Science 2008, 320(5872):77-82.
• [16]Pyle AM: The tertiary structure of group II introns: implications for biological function and evolution. Crit Rev Biochem Mol Biol 2010, 45(3):215-232.
• [17]Stabell FB, Tourasse NJ, Kolstø AB: A conserved 3' extension in unusual group II introns is important for efficient second-step splicing. Nucleic Acids Res 2009, 37(10):3202-3214.
• [18]Tourasse NJ, Stabell FB, Kolstø AB: Structural and functional evolution of group II intron ribozymes: insights from unusual elements carrying a 3' extension. N Biotechnol 2010, 27(3):204-211.
• [19]Tourasse NJ, Stabell FB, Reiter L, Kolstø AB: Unusual group II introns in bacteria of the Bacillus cereus group. J Bacteriol 2005, 187(15):5437-5451.
• [20]Helgason E, Økstad OA, Caugant DA, Johansen HA, Fouet A, Mock M, Hegna I, Kolsto AB: Bacillus anthracis, Bacillus cereus, and Bacillus thuringiensis-one species on the basis of genetic evidence. Appl Environ Microbiol 2000, 66(6):2627-2630.
• [21]Kolstø AB, Tourasse NJ, Økstad OA: What sets Bacillus anthracis apart from other Bacillus species? Annu Rev Microbiol 2009, 63:451-476.
• [22]Rasko DA, Altherr MR, Han CS, Ravel J: Genomics of the Bacillus cereus group of organisms. FEMS Microbiol Rev 2005, 29(2):303-329.
• [23]Tourasse NJ, Helgason E, Økstad OA, Hegna IK, Kolstø AB: The Bacillus cereus group: novel aspects of population structure and genome dynamics. J Appl Microbiol 2006, 101(3):579-593.
• [24]Stabell FB, Tourasse NJ, Ravnum S, Kolstø AB: Group II intron in Bacillus cereus has an unusual 3' extension and splices 56 nucleotides downstream of the predicted site. Nucleic Acids Res 2007, 35(5):1612-1623.
• [25]Takami H, Krulwich TA: Reidentification of facultatively alkaliphilic Bacillus firmus OF4 as Bacillus pseudofirmus OF4. Extremophiles 2000, 4(1):19-22.
• [26]Goto K, Omura T, Hara Y, Sadaie Y: Application of the partial 16S rDNA sequence as an index for rapid identification of species in the genus Bacillus. J Gen Appl Microbiol 2005, 46(1):1-8.
• [27]Grynberg M, Li Z, Szczurek E, Godzik A: Putative type IV secretion genes in Bacillus anthracis. Trends Microbiol 2007, 15(5):191-195.
• [28]Rasko DA, Rosovitz MJ, Økstad OA, Fouts DE, Jiang L, Cer RZ, Kolstø AB, Gill SR, Ravel J: Complete sequence analysis of novel plasmids from emetic and periodontal Bacillus cereus isolates reveals a common evolutionary history among the B. cereus-group plasmids, including Bacillus anthracis pXO1. J Bacteriol 2007, 189(1):52-64.
• [29]Tourasse NJ, Økstad OA, Kolstø AB: HyperCAT: an extension of the SuperCAT database for global multi-scheme and multi-datatype phylogenetic analysis of the Bacillus cereus group population. Database (Oxford) 2010., 2010baq017
• [30]Dai L, Toor N, Olson R, Keeping A, Zimmerly S: Database for mobile group II introns. Nucleic Acids Res 2003, 31(1):424-426.
• [31]Benson DA, Karsch-Mizrachi I, Lipman DJ, Ostell J, Sayers EW: GenBank. Nucleic Acids Res 2011, (39 Database):D32-D37.
• [32]Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ: Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 1997, 25(17):3389-3402.
• [33]Tourasse NJ, Kolstø AB: SuperCAT: a supertree database for combined and integrative multilocus sequence typing analysis of the Bacillus cereus group of bacteria (including B. cereus, B. anthracis and B. thuringiensis). Nucleic Acids Res 2008, (36 Database):D461-D468.
• [34]Zuker M: Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res 2003, 31(13):3406-3415.
• [35]Markham NR, Zuker M: UNAFold: software for nucleic acid folding and hybridization. Methods Mol Biol 2008, 453:3-31.
• [36]Toor N, Hausner G, Zimmerly S: Coevolution of group II intron RNA structures with their intron-encoded reverse transcriptases. RNA 2001, 7(8):1142-1152.
• [37]Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, et al.: Clustal W and Clustal × version 2.0. Bioinformatics 2007, 23(21):2947-2948.
• [38]Thompson JD, Higgins DG, Gibson TJ: CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 1994, 22(22):4673-4680.
• [39]Gouy M, Guindon S, Gascuel O: SeaView version 4: a multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Mol Biol Evol 2010, 27(2):221-224.
• [40]Galtier N, Gouy M, Gautier C: SEAVIEW and PHYLO_WIN: two graphic tools for sequence alignment and molecular phylogeny. Comput Appl Biosci 1996, 12(6):543-548.
• [41]Saitou N, Nei M: The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 1987, 4(4):406-425.
• [42]Tamura K: Estimation of the number of nucleotide substitutions when there are strong transition-transversion and G+C-content biases. Mol Biol Evol 1992, 9(4):678-687.
• [43]Felsenstein J: Confidence limits on phylogenies: an approach using the bootstrap. Evolution 1985, 39:783-791.
• [44]Tamura K, Dudley J, Nei M, Kumar S: MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 2007, 24(8):1596-1599.
• [45]Hill KK, Ticknor LO, Okinaka RT, Asay M, Blair H, Bliss KA, Laker M, Pardington PE, Richardson AP, Tonks M, et al.: Fluorescent amplified fragment length polymorphism analysis of Bacillus anthracis, Bacillus cereus, and Bacillus thuringiensis isolates. Appl Environ Microbiol 2004, 70(2):1068-1080.
• [46]Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O: New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 2010, 59:307-321.
• [47]Guindon S, Gascuel O: A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 2003, 52(5):696-704.
• [48]Felsenstein J, Churchill GA: A hidden markov model approach to variation among sites in rate of evolution. Mol Biol Evol 1996, 13(1):93-104.
• [49]Anisimova M, Gascuel O: Approximate likelihood-ratio test for branches: a fast, accurate, and powerful alternative. Syst Biol 2006, 55(4):539-552.