Secondary loss of a cis-spliced intron during the divergence of Giardia intestinalis assemblages

BMC Research Notes

Tetsuo Hashimoto²  Yuji Inagaki²  Ryoma Kamikawa¹ 

[1] Graduate School of Global Environmental Studies, Kyoto University, Kyoto, Japan;Centre for Computational Sciences, University of Tsukuba, Tsukuba, Ibaraki, Japan

关键词: Reverse transcription;    Reduced genome;    Homologous recombination;    Intron loss;   

Others  :  826374
DOI  :  10.1186/1756-0500-7-413

 received in 2013-11-19, accepted in 2014-06-20,  发布年份 2014

【 摘 要 】

Background

Giardia intestinalis is a parasitic unicellular eukaryote with a highly reduced genome, in which only six cis-spliced and four trans-spliced introns have been discovered. However, we anticipate that more cis- and trans-spliced introns likely remain unidentified in genes encoding hypothetical proteins that occupy ca. 2/3 of all of the open reading frames (ORFs) in the Giardia genome. Consequently, comprehensive surveys of introns in ORFs for hypothetical proteins are critical for better understanding of the intron evolution in this organism.

Results

In this study, we identified two novel cis-spliced introns in the draft genome data of G. intestinalis strain WB, by surveying the conserved sequence motifs shared amongst the previously known introns. G. intestinalis strains can be divided into phylogenetically distinct assemblages A–H, and all the introns identified in past studies are shared among the published genome data from strains WB, DH, GS, and P15 representing assemblages A1, A2, B, and E, respectively. Nevertheless one of the two novel introns identified in this study was found to be absent in strain P15.

Conclusion

By considering the organismal relationship among G. intestinalis assemblages A1, A2, B, and E, one of the two introns identified in this study has highly likely been lost after the divergence of the assemblages. On the basis of a sequence comparison between the intron-bearing loci in WB, DH, and GS genomes and the homologous but intron-free locus in P15 genome, we propose that the loss of this particular intron was mediated by integration of the DNA fragment reverse-transcribed from mature mRNAs.

【 授权许可】

   
2014 Kamikawa et al.; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 2.

【 参考文献 】

• [1]Wahl MC, Will CL, Lührmann R: The spliceosome: design principles of a dynamic RNP machine. Cell 2009, 136:701-718.
• [2]Keeling PJ, Slamovits CH: Causes and effects of nuclear genome reduction. Curr Opn Genet Dev 2005, 15:601-608.
• [3]Rodriguez-Trelles F, Tarrio R, Ayala FJ: Origins and evolution of spliceosomal introns. Annu Rev Genet 2006, 40:47-76.
• [4]Morrison HG, McArthur AG, Gillin FD, Aley SB, Adam RD, Olsen GJ, Best AA, Cande WZ, Chen F, Cipriano MJ, Davids BJ, Dawson SC, Elmendorf HG, Hehl AB, Holder ME, Huse SM, Kim UU, Lasek-Nesselquist E, Manning G, Nigam A, Nixon JE, Palm D, Passamaneck NE, Prabhu A, Reich CI, Reiner DS, Samuelson J, Svard SG, Sogin ML: Genomic minimalism in the early diverging intestinal parasite Giardia lamblia. Science 2007, 317:1921-1926.
• [5]Nixon JE, Wang A, Morrison HG, McArthur AG, Sogin ML, Loftus BJ, Samuelson J: A spliceosomal intron in Giardia lamblia. Proc Natl Acad Sci U S A 2002, 99:3701-3705.
• [6]Russell AG, Shutt TE, Watkins RF, Gray MW: An ancient spliceosomal intron in the ribosomal protein L7a gene (Rpl7a) of Giardia lamblia. BMC Evol Biol 2005, 5:45.
• [7]Kamikawa R, Inagaki Y, Tokoro M, Roger AJ, Hashimoto T: Split introns in the genome of Giardia intestinalis are excised by spliceosome-mediated trans-splicing. Curr Biol 2011, 21:311-315.
• [8]Kamikawa R, Inagaki Y, Roger AJ, Hashimoto T: Splintrons in Giardia intestinalis: spliceosomal introns in a split form. Comm Integr Biol 2011, 4:454-456.
• [9]Nageshan RK, Roy N, Hehl AB, Tatu U: Post-transcriptional repair of a split heat shock protein 90 gene by mRNA trans-splicing. J Biol Chem 2011, 286:7116-7122.
• [10]Kamikawa R, Inagaki Y, Hashimoto T: A novel spliceosome-mediated trans-splicing can change our view on genome complexity of the divergent eukaryote Giardia intestinalis. Biophys Rev 2012, 3:193-197.
• [11]Roy SW, Hudson AJ, Joseph J, Yee J, Russell AG: Numerous fragmented spliceosomal introns, AT-AC splicing, and an unusual dynein gene expression pathway in Giardia lamblia. Mol Biol Evol 2012, 29:43-49.
• [12]Franzén O, Jerlström-Hultqvist J, Einarsson E, Ankarklev J, Ferella M, Andersson B, Svärd SG: Transcriptome profiling of Giardia intestinalis using strand-specific RNA-Seq. PLoS Comput Biol 2013, 9:e1003000.
• [13]Adam RD, Dahlstrom EW, Martens CA, Bruno DP, Barbian KD, Ricklefs SM, Hernandez MM, Narla NP, Patel RB, Porcella SF, Nash TE: Genome sequencing of Giardia lamblia genotypes A2 and B isolates (DH and GS) and comparative analysis with the genomes of genotypes A1 and E (WB and Pig). Genome Biol Evol 2013, 5:2498-2511.
• [14]Franzén O, Jerlström-Hultqvist J, Castro E, Sherwood E, Ankarklev J, Reiner DS, Palm D, Andersson JO, Andersson B, Svärd SG: Draft genome sequencing of Giardia intestinalis assemblage B isolate GS: Is human giardiasis caused by two different species? PLoS Pathog 2009, 5:e1000560.
• [15]Jerlström-Hultqvist J, Franzén O, Ankarklev J, Xu F, Nohynkova E, Andersson JO, Svard SG, Andersson B: Genome analysis and comparative genomics of a Giardia intestinalis assemblage E isolate. BMC Genomics 2010, 11:543.
• [16]Kamikawa R, Nishimura H, Sako Y: Analysis of the mitochondrial genome, transcripts, and electron transport activity in the dinoflagellate Alexandrim catenella (Gonyaulacales, Dinophyceae). Phycol Res 2009, 57:1-11.
• [17]Lasek-Nesselquista E, Welch DM, Sogin ML: The identification of a new Giardia duodenalis assemblage in marine vertebrates and a preliminary analysis of G. duodenalis population biology in marine systems. Int J Parasitol 2010, 40:1063-1074.
• [18]Nash TE, Keister DB: Differences in excretory-secretory products and surface antigens among 19 isolates of Giardia. J Infect Dis 1985, 152:1166-1171.
• [19]Monis PT, Andrews RH, Mayrhofer G, Ey PL: Molecular systematics of the parasitic protozoan Giardia intestinalis. Mol Biol Evol 1999, 16:1135-1144.
• [20]Monis PT, Caccio SM, Thompson RCA: Variation in Giardia: towards a taxonomic revision of the genus. Trends Parasiol 2009, 25:93-100.
• [21]Roy SW, Gilbert W: The evolution of spliceosomal introns: patterns, puzzles and progress. Nat Rev Genet 2006, 7:211-221.
• [22]Farlow A, Meduri E, Schlotterer C: DNA double-strand break repair and the evolution of intron density. Trends Genet 2011, 27:1-6.
• [23]Cohen NE, Shen R, Carmel L: The role of reverse transcriptase in intron gain and loss mechanisms. Mol Biol Evol 2012, 29:179-186.
• [24]Burke WD, Malik HS, Rich SM, Eickbush TH: Ancient lineages of non-LTR retrotransposons in the primitive eukaryote, Giardia lamblia. Mol Biol Evol 2002, 19:619-630.