Evolutionary and biogeographical implications of degraded LAGLIDADG endonuclease functionality and group I intron occurrence in stony corals (Scleractinia) and mushroom corals (Corallimorpharia)

Celis JS, Edgell DR, Stelbrink B, Wibberg D, Hauffe T, Blom J, Kalinowski J, Wilke T (2017)
PLOS ONE 12(3): e0173734.

Zeitschriftenaufsatz | Veröffentlicht | Englisch
 
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Autor*in
Celis, Juan Sebastian; Edgell, David R.; Stelbrink, Bjoern; Wibberg, DanielUniBi; Hauffe, Torsten; Blom, Jochen; Kalinowski, JörnUniBi; Wilke, Thomas
Abstract / Bemerkung
Group I introns and homing endonuclease genes (HEGs) are mobile genetic elements, capable of invading target sequences in intron-less genomes. LAGLIDADG HEGs are the largest family of endonucleases, playing a key role in the mobility of group I introns in a process known as 'homing'. Group I introns and HEGs are rare in metazoans, and can be mainly found inserted in the COXI gene of some sponges and cnidarians, including stony corals (Scleractinia) and mushroom corals (Corallimorpharia). Vertical and horizontal intron transfer mechanisms have been proposed as explanations for intron occurrence in cnidarians. However, the central role of LAGLIDADG motifs in intron mobility mechanisms remains poorly understood. To resolve questions regarding the evolutionary origin and distribution of group I introns and HEGs in Scleractinia and Corallimorpharia, we examined intron/HEGs sequences within a comprehensive phylogenetic framework. Analyses of LAGLIDADG motif conservation showed a high degree of degradation in complex Scleractinia and Corallimorpharia. Moreover, the two motifs lack the respective acidic residues necessary for metal-ion binding and catalysis, potentially impairing horizontal intron mobility. In contrast, both motifs are highly conserved within robust Scleractinia, indicating a fully functional endonuclease capable of promoting horizontal intron transference. A higher rate of non-synonymous substitutions (K-a) detected in the HEGs of complex Scleractinia and Corallimorpharia suggests degradation of the HEG, whereas lower K-a rates in robust Scleractinia are consistent with a scenario of purifying selection. Molecular-clock analyses and ancestral inference of intron type indicated an earlier intron insertion in complex Scleractinia and Corallimorpharia in comparison to robust Scleractinia. These findings suggest that the lack of horizontal intron transfers in the former two groups is related to an age-dependent degradation of the endonuclease activity. Moreover, they also explain the peculiar geographical patterns of introns in stony and mushroom corals.
Erscheinungsjahr
2017
Zeitschriftentitel
PLOS ONE
Band
12
Ausgabe
3
Art.-Nr.
e0173734
ISSN
1932-6203
Page URI
https://pub.uni-bielefeld.de/record/2909432

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Celis JS, Edgell DR, Stelbrink B, et al. Evolutionary and biogeographical implications of degraded LAGLIDADG endonuclease functionality and group I intron occurrence in stony corals (Scleractinia) and mushroom corals (Corallimorpharia). PLOS ONE. 2017;12(3): e0173734.
Celis, J. S., Edgell, D. R., Stelbrink, B., Wibberg, D., Hauffe, T., Blom, J., Kalinowski, J., et al. (2017). Evolutionary and biogeographical implications of degraded LAGLIDADG endonuclease functionality and group I intron occurrence in stony corals (Scleractinia) and mushroom corals (Corallimorpharia). PLOS ONE, 12(3), e0173734. doi:10.1371/journal.pone.0173734
Celis, Juan Sebastian, Edgell, David R., Stelbrink, Bjoern, Wibberg, Daniel, Hauffe, Torsten, Blom, Jochen, Kalinowski, Jörn, and Wilke, Thomas. 2017. “Evolutionary and biogeographical implications of degraded LAGLIDADG endonuclease functionality and group I intron occurrence in stony corals (Scleractinia) and mushroom corals (Corallimorpharia)”. PLOS ONE 12 (3): e0173734.
Celis, J. S., Edgell, D. R., Stelbrink, B., Wibberg, D., Hauffe, T., Blom, J., Kalinowski, J., and Wilke, T. (2017). Evolutionary and biogeographical implications of degraded LAGLIDADG endonuclease functionality and group I intron occurrence in stony corals (Scleractinia) and mushroom corals (Corallimorpharia). PLOS ONE 12:e0173734.
Celis, J.S., et al., 2017. Evolutionary and biogeographical implications of degraded LAGLIDADG endonuclease functionality and group I intron occurrence in stony corals (Scleractinia) and mushroom corals (Corallimorpharia). PLOS ONE, 12(3): e0173734.
J.S. Celis, et al., “Evolutionary and biogeographical implications of degraded LAGLIDADG endonuclease functionality and group I intron occurrence in stony corals (Scleractinia) and mushroom corals (Corallimorpharia)”, PLOS ONE, vol. 12, 2017, : e0173734.
Celis, J.S., Edgell, D.R., Stelbrink, B., Wibberg, D., Hauffe, T., Blom, J., Kalinowski, J., Wilke, T.: Evolutionary and biogeographical implications of degraded LAGLIDADG endonuclease functionality and group I intron occurrence in stony corals (Scleractinia) and mushroom corals (Corallimorpharia). PLOS ONE. 12, : e0173734 (2017).
Celis, Juan Sebastian, Edgell, David R., Stelbrink, Bjoern, Wibberg, Daniel, Hauffe, Torsten, Blom, Jochen, Kalinowski, Jörn, and Wilke, Thomas. “Evolutionary and biogeographical implications of degraded LAGLIDADG endonuclease functionality and group I intron occurrence in stony corals (Scleractinia) and mushroom corals (Corallimorpharia)”. PLOS ONE 12.3 (2017): e0173734.

1 Zitation in Europe PMC

Daten bereitgestellt von Europe PubMed Central.

Giant group I intron in a mitochondrial genome is removed by RNA back-splicing.
Chi SI, Dahl M, Emblem Å, Johansen SD., BMC Mol Biol 20(1), 2019
PMID: 31153363

69 References

Daten bereitgestellt von Europe PubMed Central.

Representation of the secondary and tertiary structure of group I introns
AUTHOR UNKNOWN, 1994

AUTHOR UNKNOWN, 2002
Learning to live together: mutualism between self-splicing introns and their hosts.
Edgell DR, Chalamcharla VR, Belfort M., BMC Biol. 9(), 2011
PMID: 21481283
Bacterial group I introns: mobile RNA catalysts.
Hausner G, Hafez M, Edgell DR., Mob DNA 5(1), 2014
PMID: 24612670
Coevolution of a homing endonuclease and its host target sequence.
Scalley-Kim M, McConnell-Smith A, Stoddard BL., J. Mol. Biol. 372(5), 2007
PMID: 17720189
Conservation of intron and intein insertion sites: implications for life histories of parasitic genetic elements.
Swithers KS, Senejani AG, Fournier GP, Gogarten JP., BMC Evol. Biol. 9(), 2009
PMID: 20043855
Adaptation for horizontal transfer in a homing endonuclease.
Koufopanou V, Goddard MR, Burt A., Mol. Biol. Evol. 19(3), 2002
PMID: 11861883

AUTHOR UNKNOWN, 2006
Recurrent invasion and extinction of a selfish gene.
Goddard MR, Burt A., Proc. Natl. Acad. Sci. U.S.A. 96(24), 1999
PMID: 10570167
Rapid evolution of the DNA-binding site in LAGLIDADG homing endonucleases.
Lucas P, Otis C, Mercier JP, Turmel M, Lemieux C., Nucleic Acids Res. 29(4), 2001
PMID: 11160929
The spread of LAGLIDADG homing endonuclease genes in rDNA.
Haugen P, Bhattacharya D., Nucleic Acids Res. 32(6), 2004
PMID: 15069127
Evolution of mobile group I introns: recognition of intron sequences by an intron-encoded endonuclease.
Loizos N, Tillier ER, Belfort M., Proc. Natl. Acad. Sci. U.S.A. 91(25), 1994
PMID: 7991569
Integration of the Tetrahymena group I intron into bacterial rRNA by reverse splicing in vivo.
Roman J, Woodson SA., Proc. Natl. Acad. Sci. U.S.A. 95(5), 1998
PMID: 9482851
Invasion and persistence of a selfish gene in the Cnidaria.
Goddard MR, Leigh J, Roger AJ, Pemberton AJ., PLoS ONE 1(), 2006
PMID: 17183657
Sea anemones possess dynamic mitogenome structures.
Emblem A, Okkenhaug S, Weiss ES, Denver DR, Karlsen BO, Moum T, Johansen SD., Mol. Phylogenet. Evol. 75(), 2014
PMID: 24613805
Diversity of sponge mitochondrial introns revealed by cox 1 sequences of Tetillidae.
Szitenberg A, Rot C, Ilan M, Huchon D., BMC Evol. Biol. 10(), 2010
PMID: 20849667
Mitochondrial group I and group II introns in the sponge orders Agelasida and Axinellida.
Huchon D, Szitenberg A, Shefer S, Ilan M, Feldstein T., BMC Evol. Biol. 15(), 2015
PMID: 26653218
Mitochondrial genome of Trichoplax adhaerens supports placozoa as the basal lower metazoan phylum.
Dellaporta SL, Xu A, Sagasser S, Jakob W, Moreno MA, Buss LW, Schierwater B., Proc. Natl. Acad. Sci. U.S.A. 103(23), 2006
PMID: 16731622
Evolution of scleractinian corals inferred from molecular systematics
AUTHOR UNKNOWN, 1996
Molecular phylogenetic hypotheses for the evolution of scleractinian corals
AUTHOR UNKNOWN, 2000
Naked corals: skeleton loss in Scleractinia.
Medina M, Collins AG, Takaoka TL, Kuehl JV, Boore JL., Proc. Natl. Acad. Sci. U.S.A. 103(24), 2006
PMID: 16754865
A comprehensive phylogenetic analysis of the Scleractinia (Cnidaria, Anthozoa) based on mitochondrial CO1 sequence data.
Kitahara MV, Cairns SD, Stolarski J, Blair D, Miller DJ., PLoS ONE 5(7), 2010
PMID: 20628613
The "naked coral" hypothesis revisited--evidence for and against scleractinian monophyly.
Kitahara MV, Lin MF, Foret S, Huttley G, Miller DJ, Chen CA., PLoS ONE 9(4), 2014
PMID: 24740380
Mitochondrial genome rearrangements in the scleractinia/corallimorpharia complex: implications for coral phylogeny.
Lin MF, Kitahara MV, Luo H, Tracey D, Geller J, Fukami H, Miller DJ, Chen CA., Genome Biol Evol 6(5), 2014
PMID: 24769753
The natural history of group I introns.
Haugen P, Simon DM, Bhattacharya D., Trends Genet. 21(2), 2005
PMID: 15661357

AUTHOR UNKNOWN, 2005
Basic local alignment search tool.
Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ., J. Mol. Biol. 215(3), 1990
PMID: 2231712
Gapped BLAST and PSI-BLAST: a new generation of protein database search programs
AUTHOR UNKNOWN, 1997
Complete mitochondrial genome of the scleractinian coral Porites rus
AUTHOR UNKNOWN, 2016
State-of the art methodologies dictate new standards for phylogenetic analysis.
Anisimova M, Liberles DA, Philippe H, Provan J, Pupko T, von Haeseler A., BMC Evol. Biol. 13(), 2013
PMID: 23914788
GenDB--an open source genome annotation system for prokaryote genomes.
Meyer F, Goesmann A, McHardy AC, Bartels D, Bekel T, Clausen J, Kalinowski J, Linke B, Rupp O, Giegerich R, Puhler A., Nucleic Acids Res. 31(8), 2003
PMID: 12682369
Identifying bacterial genes and endosymbiont DNA with Glimmer.
Delcher AL, Bratke KA, Powers EC, Salzberg SL., Bioinformatics 23(6), 2007
PMID: 17237039
BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT
AUTHOR UNKNOWN, 1999
Clustal W and Clustal X version 2.0.
Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG., Bioinformatics 23(21), 2007
PMID: 17846036
HGVS Recommendations for the Description of Sequence Variants: 2016 Update.
den Dunnen JT, Dalgleish R, Maglott DR, Hart RK, Greenblatt MS, McGowan-Jordan J, Roux AF, Smith T, Antonarakis SE, Taschner PE., Hum. Mutat. 37(6), 2016
PMID: 26931183
The Phyre2 web portal for protein modeling, prediction and analysis.
Kelley LA, Mezulis S, Yates CM, Wass MN, Sternberg MJ., Nat Protoc 10(6), 2015
PMID: 25950237
MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets
AUTHOR UNKNOWN, 2016

AUTHOR UNKNOWN, 2015
DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates.
Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R., Mol. Marine Biol. Biotechnol. 3(5), 1994
PMID: 7881515
WebLogo: a sequence logo generator.
Crooks GE, Hon G, Chandonia JM, Brenner SE., Genome Res. 14(6), 2004
PMID: 15173120
Evolutionary diversification of reef corals: a comparison of the molecular and fossil records.
Simpson C, Kiessling W, Mewis H, Baron-Szabo RC, Muller J., Evolution 65(11), 2011
PMID: 22023591
Bayesian phylogenetics with BEAUti and the BEAST 1.7.
Drummond AJ, Suchard MA, Xie D, Rambaut A., Mol. Biol. Evol. 29(8), 2012
PMID: 22367748
jModelTest: phylogenetic model averaging.
Posada D., Mol. Biol. Evol. 25(7), 2008
PMID: 18397919

AUTHOR UNKNOWN, 2010

AUTHOR UNKNOWN, 0
Stochastic mapping of morphological characters.
Huelsenbeck JP, Nielsen R, Bollback JP., Syst. Biol. 52(2), 2003
PMID: 12746144
phytools: an R package for phylogenetic comparative biology (and other things)
AUTHOR UNKNOWN, 2012
A motor component to the memories of habitual foraging routes in wood ants?
Lent DD, Graham P, Collett TS., Curr. Biol. 19(2), 2009
PMID: 19135366
Homing endonuclease genes: the rise and fall and rise again of a selfish element.
Burt A, Koufopanou V., Curr. Opin. Genet. Dev. 14(6), 2004
PMID: 15531154
The structure of the protein universe and genome evolution.
Koonin EV, Wolf YI, Karev GP., Nature 420(6912), 2002
PMID: 12432406
The ancient evolutionary origins of Scleractinia revealed by azooxanthellate corals.
Stolarski J, Kitahara MV, Miller DJ, Cairns SD, Mazur M, Meibom A., BMC Evol. Biol. 11(), 2011
PMID: 22034946

AUTHOR UNKNOWN, 2002
An early Hettangian coral reef in southern France: implications for the end-Triassic reef crisis
AUTHOR UNKNOWN, 2009
On the potential for ocean acidification to be a general cause of ancient reef crises
AUTHOR UNKNOWN, 2011
Analysis of complete mitochondrial DNA sequences of three members of the Montastraea annularis coral species complex. Cnidaria, Anthozoa, Scleractinia
AUTHOR UNKNOWN, 2005
Plate tectonics drive tropical reef biodiversity dynamics.
Leprieur F, Descombes P, Gaboriau T, Cowman PF, Parravicini V, Kulbicki M, Melian CJ, de Santana CN, Heine C, Mouillot D, Bellwood DR, Pellissier L., Nat Commun 7(), 2016
PMID: 27151103
Are coral reefs victims of their own past success?
Renema W, Pandolfi JM, Kiessling W, Bosellini FR, Klaus JS, Korpanty C, Rosen BR, Santodomingo N, Wallace CC, Webster JM, Johnson KG., Sci Adv 2(4), 2016
PMID: 27152330
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