Journal of Molecular Evolution

, Volume 64, Issue 5, pp 591–600 | Cite as

Novel Group I Introns Encoding a Putative Homing Endonuclease in the Mitochondrial cox1 Gene of Scleractinian Corals

  • Hironobu Fukami
  • Chaolun Allen Chen
  • Chi-Yung Chiou
  • Nancy Knowlton
Article

Abstract

Analyses of mitochondrial sequences revealed the existence of a group I intron in the cytochrome oxidase subunit 1 (cox1) gene in 13 of 41 genera (20 out of 73 species) of corals conventionally assigned to the suborder Faviina. With one exception, phylogenies of the coral cox1 gene and its intron were concordant, suggesting at most two insertions and many subsequent losses. The coral introns were inferred to encode a putative homing endonuclease with a LAGLI-DADG motif as reported for the cox1 group I intron in the sea anemone Metridium senile. However, the coral and sea anemone cox1 group I introns differed in several aspects, such as the intron insertion site and sequence length. The coral cox1 introns most closely resemble the mitochondrial cox1 group I introns of a sponge species, which also has the same insertion site. The coral introns are also more similar to the introns of several fungal species than to that of the sea anemone (although the insertion site differs in the fungi). This suggests either a horizontal transfer between a sponge and a coral or independent transfers from a similar fungal donor (perhaps one with an identical insertion site that has not yet been discovered). The common occurrence of this intron in corals strengthens the evidence for an elevated abundance of group I introns in the mitochondria of anthozoans.

Keywords

Scleractinia Corals Mitochondria Group I intron Homing endonuclease cox1 

References

  1. Adams KL, Clements MJ, Vaughn JC (1998) The Peperomia mitochondrial coxI group I intron: timing of horizontal transfer and subsequent evolution of the intron. J Mol Evol 46:689–696PubMedCrossRefGoogle Scholar
  2. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLASZT: a new generatin of protein database search programs. Nucleic Acids Res 25:3389–3402PubMedCrossRefGoogle Scholar
  3. Beagley CT, Okada NA, Wolstenholme DR (1996) Two mitochondrial group I introns in a metazoan, the sea anemone Metridium senile: One intron contains genes for subunits 1 and 3 of NADH dehydrogenase. Proc Natl Acad Sci USA 93:5619–5623PubMedCrossRefGoogle Scholar
  4. Beagley CT, Okimoto R, Wolstenholme DR (1998) The mitochondrial genome of the sea anemone Metridium senile (Cnidaria): introns, a paucity of tRNA genes, and a near-standard genetic code. Genetics 148:1091–1108PubMedGoogle Scholar
  5. Beaton MJ, Roger AJ, Cavalier-Smith T (1998) Sequence analysis of the mitochondrial genome of Sarcophyton glaucum: conserved gene order among octocorals. J Mol Evol 47:697–708PubMedCrossRefGoogle Scholar
  6. Belfort M, Roberts RJ (1997) Homing endonucleases: keeping the house in order. Nucleic Acids Res 25:3379–3388PubMedCrossRefGoogle Scholar
  7. Bell-Pedersen D, Quirk S, Clyman J, Belfort M (1990) Intron mobility in phage T4 is dependent upon a distinctive class of endonucleases and independent of DNA sequences encoding the intron core: mechanistic and evolutionary implications. Nucleic Acids Res 18:3763–3770PubMedCrossRefGoogle Scholar
  8. Bentis CJ, Kaufman L, Golubic S (2000) Endolithic fungi in reef-building corals (order: Scleractinia) are common, cosmopolitan, and potentially pathogenic. Biol Bull 198:254–260PubMedCrossRefGoogle Scholar
  9. Bhattacharya D, Surek B, Rüsing M, Damberger S, Melkonian M (1994) Group I introns are inherited through common ancestry in the nuclear-encoded rDNA of Zygnematales (Charophyceae). Proc Natl Acad Sci USA 91:9916–9920PubMedCrossRefGoogle Scholar
  10. Bullerwell CE, Leigh J, Forget L, Lang BF (2003) A comparison of three fission yeast mitochondrial genomes. Nucleic Acids Res 31:759–768PubMedCrossRefGoogle Scholar
  11. Burke JM, Belfort M, Cech TR, Davies RW, Schweyen RJ, Shub DA, Szostak JW, Tabak HF (1987) Structural conventions for group I introns. Nucleic Acids Res 15:7217–7221PubMedCrossRefGoogle Scholar
  12. Cech TR (1988) Conserved sequences and structures of group I introns: building an active site for RNA catalysis. Gene 73:259–271PubMedCrossRefGoogle Scholar
  13. Cech TR, Damberger SH, Gutell RR (1994) Representation of the secondary and tertiary structure of group I introns. Nat Struct Biol 1:273–280PubMedCrossRefGoogle Scholar
  14. Chen CA, Wallace CC, Wolstenholme J (2002) Analysis of mitochondrial 12S RNA gene supports a two-clade hypothesis of the evolutionary history of scleractinian corals. Mol Phylogenet Evol 23:137–149PubMedCrossRefGoogle Scholar
  15. Cho Y, Qio Y, Kuhlman P, Palmer JD (1998) Explosive invasion of plant mitochondria by a group I intron. Proc Natl Acad Sci USA 95:14244–14249PubMedCrossRefGoogle Scholar
  16. Dujon B (1989) Group I intron as mobile genetic elements: facts and mechanistic speculations. Gene 82:91–114PubMedCrossRefGoogle Scholar
  17. Edgell DR, Belfort M, Shub DA (2000) Barriers to intron promiscuity in bacteria. J Bacteriol 182:5281–5289PubMedCrossRefGoogle Scholar
  18. Felsenstein J (1978) Cases in which parsimony or compatibility methods will be positively misleading. Syst Zool 27:401–410CrossRefGoogle Scholar
  19. Fukami H, Knowlton N (2005) Analysis of complete mitochondrial DNA sequences of three members of the Montastraea annularis coral species complex (Cnidaria, Anthozoa, Scleractinia). Coral Reefs 24:410–417CrossRefGoogle Scholar
  20. Fukami H, Budd AF, Levitan DR, Jara J, Kersanach R, Knowlton N (2004a) Geographic differences in species boundaries among members of the Montastraea annularis complex based on molecular and morphological markers. Evolution 58:324–337CrossRefGoogle Scholar
  21. Fukami H, Budd AF, Paulay G, Sole-Cava A, Chen CA, Iwao K, Knowlton N (2004b) Conventional taxonomy obscures deep divergence between Pacific and Atlantic corals. Nature 427:832–835CrossRefGoogle Scholar
  22. Kuhsel MG, Strickland R, Palmer JD (1990) An ancient group I intron shared by eubacteria and chloroplasts. Science 250:1570–1573PubMedCrossRefGoogle Scholar
  23. Lambowitz AM, Belfort M (1993) Introns as mobile genetic elements. Annu Rev Biochem 62:587–622PubMedCrossRefGoogle Scholar
  24. Le Campion-Alsumard T, Golubic S, Priess K (1995) Fungi in corals: symbiosis or disease: interaction between polyps and fungi causes pearl-like skeleton biomineralization. Mar Ecol Prog Ser 117:137–147Google Scholar
  25. Lisacek F, Diaz Y, Michel F (1994) Automatic identification of group I intron cores in genomic DNA sequences. J Mol Biol 235:1206–1217PubMedCrossRefGoogle Scholar
  26. Loizos N, Tillier ERM, Belfort M (1994) Evolution of mobile group I introns: Recognition of intron sequences by an intron-encoded endonuclease. Proc Natl Acad Sci USA 91:11983–11987PubMedCrossRefGoogle Scholar
  27. López-Victoria M, Zea S (2004) Storm-mediated coral colonization by an excavating Caribbean sponge. Clim Res 26:251–256Google Scholar
  28. Medina M, Weil E, Szmant AM (1999) Examination of the Montastraea annularis species complex (Cnidaria, Scleractinia) using ITS and COI sequences. Mar Biotech 1:89–97CrossRefGoogle Scholar
  29. Medina M, Collins AG, Takaoka TL, Kuehl JV, Boore JL (2006) Naked corals: Skeleton loss in Scleractinia. Proc Natl Acad Sci USA 103:9096–9100PubMedCrossRefGoogle Scholar
  30. Michel F, Westhof E (1990) Modelling of the three-dimensional architecture of group I catalytic introns based on comparative sequence analysis. J Mol Biol 216:585–610PubMedCrossRefGoogle Scholar
  31. Pearson WR, Lipman DJ (1988) Improved tools for biological sequence comparison. Proc Natl Acad Sci USA 85:2444–2448PubMedCrossRefGoogle Scholar
  32. Pont-Kingdon GA, Okada NA, Macfarlane JL, Beagley CT, Wolstenholme DR, Cavalier-Smith T, Clark-Walker GD (1995) A coral mitochondrial mutS gene. Nature 375:109–111PubMedCrossRefGoogle Scholar
  33. Pont-Kingdon G, Okada NA, Macfarlane JL, Beagley CT, Watkins-Sims CD, Cavalier-Smith T, Clark-Walker GD, Wolstenholme DR (1998) Mitochondrial DNA of the coral Sarcophyton glaucum contains a gene for a homologue of bacterial MutS: a possible case of gene transfer from the nucleus to the mitochondrion. J Mol Evol 46:419–431PubMedCrossRefGoogle Scholar
  34. Posada D, Crandall KA (1988) Modeltest: testing the model of DNA substitution. Bioinformatics 14:817–818CrossRefGoogle Scholar
  35. Raghukumar C, Raghukumar S (1991) Fungal invasion of massive corals. Mar Ecol 12:251–260Google Scholar
  36. Reinhold-Hurek B, Shub DA (1992) Self-splicing introns in tRNA genes of widely divergent bacteria. Nature 357:173–176PubMedCrossRefGoogle Scholar
  37. Romano SL, Cairns SD (2000) Molecular phylogenetic hypotheses for the evolution of scleractinian corals. Bull Mar Sci 67:1043–1068Google Scholar
  38. Romano SL, Palumbi SR (1997) Molecular evolution of a portion of the mitochondrial 16S ribosomal gene region in scleractinian corals. J Mol Evol 45:397–411PubMedCrossRefGoogle Scholar
  39. Rot C, Goldfarb I, Ilan M, Huchon D (2006) Putative cross-kingdom horizontal gene transfer in sponge (Porifera) mitochondria. BMC Evol Biol 6:71PubMedCrossRefGoogle Scholar
  40. Schönberg CHL, Wilkinson CR (2001) Induced colonization of corals by a clionid bioeroding sponge. Coral Reefs 20:69–76CrossRefGoogle Scholar
  41. Seif E, Leigh J, Liu Y, Roewer I, Forget L, Lang BF (2005) Comparative mitochondrial genomics in zygomycetes: bacteria-like RNase P RNAs, mobile elements and a close source of the group I intron invasion in angiosperms. Nucleic Acids Res 33:734–744PubMedCrossRefGoogle Scholar
  42. Shearer TL, van Oppen MJH, Romano SLR, Wörheide G (2002) Slow mitochondrial DNA sequence evolution in the Anthozoa (Cnidaria). Mol Ecol 11:2475–2487PubMedCrossRefGoogle Scholar
  43. Swofford DL (2002) PAUP*. Phylogenetic analysis using parsimony (*and other methods), version 4.0b10. Sinauer Associates, Sunderland, MAGoogle Scholar
  44. Tseng CC, Wallace CC, Chen CA (2005) Mitogenomic analysis of Montipora cactus and Anacropora matthai (Cnidaria; Scleractinia; Acroporidae) indicates an unequal rate of mitochondrial evolution among Acroporidae corals. Coral Reefs 24:502–508CrossRefGoogle Scholar
  45. van Oppen MJH, Olsen JL, Stam WT (1993) Evidence for independent acquisition of group I introns in green algae. Mol Biol Evol 10:1317–1326PubMedGoogle Scholar
  46. van Oppen MJH, Willis BL, Miller DJ (1999a) Atypically low rate of cytochrome b evolution in the scleractinian coral genus Acropora. Proc R Soc Lond B 266:179–183CrossRefGoogle Scholar
  47. van Oppen MJH, Hislop NR, Hagerman PJ, Miller DJ (1999b) Gene content and organization in a segment of the mitochondrial genome of the scleractinian coral Acropora tenuis: major differences in gene order within the anthozoan subclass Zoantharia. Mol Biol Evol 16:1812–1815Google Scholar
  48. van Oppen MJH, Catmull J, McDonald BJ, Hislop NR, Hagerman PJ, Miller DJ (2002) The mitochondrial genome of Acropora tenuis (Cnidaria; Scleractinia) contains a large group I intron and a candidate control region. J Mol Evol 55:1–13PubMedCrossRefGoogle Scholar
  49. Vaughn JC, Mason MT, Sper-Whitis GL, Kuhlman P, Palmer JD (1995) Fungal origin by horizontal transfer of a plant mitochondrial group I intron in the chimeric CoxI gene of Peperomia. J Mol Evol 41:563–572PubMedCrossRefGoogle Scholar
  50. Woo PC, Zhen H, Cai JJ, Yu J, Lau SK, Wang J, Teng JL, Wong SS, Tse RH, Chen R, Yang H, Liu B, Yuen KY (2003) The mitochondrial genome of the thermal dimorphic fungus Penicillium marneffei is more closely related to those of molds than yeasts. FEBS Lett 555:469–477PubMedCrossRefGoogle Scholar
  51. Zuker M (2003) Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res 31:3406–3415PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2007

Authors and Affiliations

  • Hironobu Fukami
    • 1
    • 4
  • Chaolun Allen Chen
    • 2
  • Chi-Yung Chiou
    • 2
  • Nancy Knowlton
    • 1
    • 3
  1. 1.Center for Marine Biodiversity and ConservationScripps Institution of Oceanography, University of California San DiegoLa JollaUSA
  2. 2.Research Centre for Biodiversity, Academia SinicaTaipeiTaiwan
  3. 3.Smithsonian Tropical Research InstitutePanamaRepública de Panamá
  4. 4.Seto Marine Biological Laboratory, Field Science Education and Research Center, Kyoto UniversityWakayamaJapan

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