Wide Occurrence of SSU rDNA Intragenomic Polymorphism in Foraminifera and its Implications for Molecular Species Identification

Protist

Volumn 165, Issue 5, 2014, Pages 645-661

  Weber, Alexandra Anh Thu ^a,b   Pawlowski, Jan ^a  

^a UNIVERSITY OF GENEVA   (Switzerland)

^b AVIGNON UNIVERSITÉ   (France)

Author keywords

DNA barcoding; Foraminifera; Intragenomic variability; Protists; SSU rDNA

Indexed keywords

PROTOZOAL DNA; RIBOSOME DNA; RNA 18S;

CHEMICAL STRUCTURE; CHEMISTRY; CLASSIFICATION; CLUSTER ANALYSIS; CONFORMATION; DNA SEQUENCE; FORAMINIFER; GENETIC VARIABILITY; GENETICS; MOLECULAR GENETICS; PHYLOGENY;

CLUSTER ANALYSIS; DNA, PROTOZOAN; DNA, RIBOSOMAL; FORAMINIFERA; GENETIC VARIATION; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; NUCLEIC ACID CONFORMATION; PHYLOGENY; RNA, RIBOSOMAL, 18S; SEQUENCE ANALYSIS, DNA;

EID: 84908127742     PISSN: 14344610     EISSN: 16180941     Source Type: Journal    
DOI: 10.1016/j.protis.2014.07.006     Document Type: Article

References (105)

1. Alper I., Frenette M., Labrie S. Ribosomal DNA polymorphisms in the yeast Geotrichum candidum. Fungal Biol 2011, 115:1259-1269.
2. Álvarez I., Wendel J.F. Ribosomal ITS sequences and plant phylogenetic inference. Mol Phylogenet Evol 2003, 29:417-434.
3. Alverson A.J. Molecular systematics and the diatom species. Protist 2008, 159:339-353.
4. Alverson A.J., Kolnick L. Intragenomic nucleotide polymorphism among small subunit (18s) rDNA paralogs in the diatom genus Skeletonema (bacillariophyta). J Phycol 2005, 41:1248-1257.
5. Andreasen K., Baldwin B.G. Nuclear ribosomal DNA sequence polymorphism and hybridization in checker mallows (Sidalcea, Malvaceae). Mol Phylogenet Evol 2003, 29:563-581.
6. Bass D., Howe A.T., Mylnikov A.P., Vickerman K., Chao E.E., Edwards Smallbone J., Snell J., Cabral C., Cavalier-Smith T. Phylogeny and classification of Cercomonadida (Protozoa, Cercozoa): Cercomonas, Eocercomonas, Paracercomonas, and Cavernomonas gen. nov. Protist 2009, 160:483-521.
7. Behnke A., Friedl T., Chepurnov V.A., Mann D.G. Reproductive compatibility and rDNA sequence analyses in the Sellaphora pupula species complex (Bacillariophyta). J Phycol 2004, 40:193-208.
8. Bik H.M., Fournier D., Sung W., Bergeron R.D., Thomas W.K. Intra-genomic variation in the ribosomal repeats of nematodes. PLoS ONE 2013, 8:e78230.
9. Bobola M.S., Smith D.E., Klein A.S. Five major nuclear ribosomal repeats represent a large and variable fraction of the genomic DNA of Picea rubens and P. mariana. Mol Biol Evol 1992, 9:125-137.
10. Boucher Y., Douady C.J., Sharma A.K., Kamekura M., Doolittle W.F. Intragenomic heterogeneity and intergenomic recombination among haloarchaeal rRNA genes. J Bacteriol 2004, 186:3980-3990.
11. Campbell C.S., Wojciechowski M.F., Baldwin B.G., Alice L.A., Donoghue M.J. Persistent nuclear ribosomal DNA sequence polymorphism in the Amelanchier agamic complex (Rosaceae). Mol Biol Evol 1997, 14:81-90.
12. Caron D.A., Countway P.D., Savai P., Gast R.J., Schnetzer A., Moorthi S.D., Dennett M.R., Moran D.M., Jones A.C. Defining DNA-based operational taxonomic units for microbial-eukaryote ecology. Appl Environ Microbiol 2009, 75:5797-5808.
13. Carranza S., Giribet G., Ribera C., Baguñà, Riutort M. Evidence that two types of 18S rDNA coexist in the genome of Dugesia (Schmidtea) mediterranea (Platyhelminthes, Turbellaria, Tricladida). Mol Biol Evol 1996, 13:824-832.
14. Casteleyn G., Adams N.G., Vanormelingen P., Debeer A.-E., Sabbe K., Vyverman W. Natural hybrids in the marine diatom Pseudo-nitzschia pungens (Bacillariophyceae): Genetic and morphological evidence. Protist 2009, 160:343-354.
15. Chenuil A., Egea E., Rocher C., Touzet H., Féral J.-P. Does hybridization increase evolutionary rate? Data from the 28S-rDNA D8 domain in echinoderms. J Mol Evol 2008, 67:539-550.
16. Ciardo D.E., Schär G., Böttger E.C., Altwegg M., Bosshard P.P. Internal transcribed spacer sequencing versus biochemical profiling for identification of medically important yeasts. J Clin Microbiol 2006, 44:77-84.
17. Cohan F.M. What are bacterial species?. Annu Rev Microbiol 2002, 56:457-487.
18. Crease T.J., Lynch M. Ribosomal DNA variation in Daphnia pulex. Mol Biol Evol 1991, 8:620-640.
19. Darty K., Denise A., Ponty Y. VARNA: Interactive drawing and editing of the RNA secondary structure. Bioinformatics 2009, 25:1974-1975.
20. Decelle J., Martin P., Paborstava K., Pond D.W., Tarling G., Mahé F., de Vargas C., Lampitt R., Not F. Diversity, ecology and biogeochemistry of cyst-forming Acantharia (Radiolaria) in the oceans. PLoS ONE 2013, 8:e53598.
21. Dover G. Molecular drive: a cohesive mode of species evolution. Nature 1982, 299:111-117.
22. Dover G.A. Linkage disequilibrium and molecular drive in the rDNA gene family. Genetics 1989, 122:249-252.
23. Edgar R.C. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 2004, 32:1792-1797.
24. Elder J.F., Turner B.J. Concerted evolution of repetitive DNA sequences in eukaryotes. Q Rev Biol 1995, 70:297-320.
25. Escobar D., Zea S., Sánchez J.A. Phylogenetic relationships among the Caribbean members of the Cliona viridis complex (Porifera, Demospongiae, Hadromerida) using nuclear and mitochondrial DNA sequences. Mol Phylogenet Evol 2012, 64:271-284.
26. Evans K.M., Wortley A.H., Mann D.G. An assessment of potential diatom "barcode" genes (cox1, rbcL, 18S and ITS rDNA) and their effectiveness in determining relationships in Sellaphora (Bacillariophyta). Protist 2007, 158:349-364.
27. Fiore-Donno A.M., Kamono A., Chao E.E., Fukui M., Cavalier-Smith T. Invalidation of Hyperamoeba by transferring its species to other genera of Myxogastria. J Eukaryot Microbiol 2010, 57:189-196.
28. Gandolfi A., Bonilauri P., Rossi V., Menozzi P. Intraindividual and intraspecies variability of ITS1 sequences in the ancient asexual Darwinula stevensoni (Crustacea: Ostracoda). Heredity 2001, 87:449-455.
29. Gaut B.S., Tredway L.P., Kubik C., Gaut R.L., Meyer W. Phylogenetic relationships and genetic diversity among members of the Festuca-Lolium complex (Poaceae) based on ITS sequence data. Plant Syst Evol 2000, 224:33-53.
30. Gernandt D.S., Liston A., Piñero D. Variation in the nrDNA ITS of Pinus subsection Cembroides: Implications for molecular systematic studies of pine species complexes. Mol Phylogenet Evol 2001, 21:449-467.
31. Glöckner G., Hülsmann N., Schleicher M., Noegel A.A., Eichinger L., Gallinger C., Pawlowski J., Sierra R., Euteneuer U., Pillet L., et al. The genome of the foraminiferan Reticulomyxa filosa. Curr Biol 2014, 24:11-18.
32. Gong J., Dong J., Liu X., Massana R. Extremely high copy numbers and polymorphisms of the rDNA operon estimated from single cell analysis of oligotrich and peritrich ciliates. Protist 2013, 164:369-379.
33. 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, 27:221-224.
34. Gribble K.E., Anderson D.M. High intraindividual, intraspecific, and interspecific variability in large-subunit ribosomal DNA in the heterotrophic dinoflagellates Protoperidinium, Diplopsalis, and Preperidinium (Dinophyceae). Phycologia 2007, 46:315-324.
35. Gunderson J.H., Sogin M.L., Wollett G., Hollingdale M., Cruz V., de la Waters A.P., McCutchan T.F. Structurally distinct, stage-specific ribosomes occur in Plasmodium. Science 1987, 238:933-937.
36. Hall T.A. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 1999, 41:95-98.
37. Hartmann S., Nason J.D., Bhattacharya D. Extensive ribosomal DNA genic variation in the columnar cactus Lophocereus. J Mol Evol 2001, 53:124-134.
38. Hillis D.M., Dixon M.T. Ribosomal DNA: molecular evolution and phylogenetic inference. Q Rev Biol 1991, 66:411-453.
39. Holzmann M., Piller W., Pawlowski J. Sequence variations in the large-subunit ribosomal RNA gene of Ammonia (foraminifera, protozoa) and their evolutionary implications. J Mol Evol 1996, 43:145-151.
40. Howe A.T., Bass D., Chao E.E., Cavalier-Smith T. New genera, species, and improved phylogeny of Glissomonadida (Cercozoa). Protist 2011, 162:710-722.
41. Howe A.T., Bass D., Scoble J.M., Lewis R., Vickerman K., Arndt H., Cavalier-Smith T. Novel cultured protists identify deep-branching environmental DNA clades of Cercozoa: New genera Tremula, Micrometopion, Minimassisteria, Nudifila, Peregrinia. Protist 2011, 162:332-372.
42. Huse S.M., Huber J.A., Morrison H.G., Sogin M.L., Welch D.M. Accuracy and quality of massively parallel DNA pyrosequencing. Genome Biol 2007, 8:R143.
43. Ironside J.E. Diversity and recombination of dispersed ribosomal DNA and protein coding genes in Microsporidia. PLoS ONE 2013, 8:e55878.
44. Izzo A., Agbowo J., Bruns T.D. Detection of plot-level changes in ectomycorrhizal communities across years in an old-growth mixed-conifer forest. New Phytol 2005, 166:619-630.
45. Jellen E.N., Phillips R.L., Rines H.W. Chromosomal localization and polymorphisms of ribosomal DNA in oat (Avena spp.). Genome 1994, 37:23-32.
46. Jobst J., King K., Hemleben V. Molecular evolution of the internal transcribed spacers (ITS1 and ITS2) and phylogenetic relationships among species of the family Cucurbitaceae. Mol Phylogenet Evol 1998, 9:204-219.
47. Karvonen P., Savolainen O. Variation in inheritance of ribosomal DNA in Pinus sylvestris L. (Scots pine). Heredity 1993, 71:614-622.
48. Ko K.S., Jung H.S. Three nonorthologous ITS1 types are present in a polypore fungus Trichaptum abietinum. Mol Phylogenet Evol 2002, 23:112-122.
49. Králová-Hromadová I., Bazsalovicsová E., Oros M., Scholz T. Sequence structure and intragenomic variability of ribosomal ITS2 in monozoic tapeworms of the genus Khawia (Cestoda: Caryophyllidea), parasites of cyprinid fish. Parasitol Res 2012, 111:1621-1627.
50. Krieger J., Fuerst P.A. Evidence of multiple alleles of the nuclear 18S ribosomal RNA gene in sturgeon (Family: Acipenseridae). J Appl Ichthyol 2002, 18:290-297.
51. Kunin V., Engelbrektson A., Ochman H., Hugenholtz P. Wrinkles in the rare biosphere: pyrosequencing errors can lead to artificial inflation of diversity estimates. Environ Microbiol 2010, 12:118-123.
52. Lanfranco L., Delpero M., Bonfante P. Intrasporal variability of ribosomal sequences in the endomycorrhizal fungus Gigaspora margarita. Mol Ecol 1999, 8:37-45.
53. Lecroq B., Lejzerowicz F., Bachar D., Christen R., Esling P., Baerlocher L., Østerås M., Farinelli L., Pawlowski J. Ultra-deep sequencing of foraminiferal microbarcodes unveils hidden richness of early monothalamous lineages in deep-sea sediments. Proc Natl Acad Sci USA 2011, 108:13177-13182.
54. Biology of Foraminifera 1991, 368. Academic Press, New York. J.J. Lee, O.R. Anderson (Eds.).
55. Lejzerowicz F., Voltsky I., Pawlowski J. Identifying active foraminifera in the Sea of Japan using metatranscriptomic approach. Deep Sea Res Part II Top Stud Oceanogr 2013, 86-87:214-220.
56. Liao D. Concerted evolution: molecular mechanism and biological implications. Am J Hum Genet 1999, 64:24-30.
57. Librado P., Rozas J. DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 2009, 25:1451-1452.
58. Linares A.R., Bowen T., Dover G.A. Aspects of nonrandom turnover involved in the concerted evolution of intergenic spacers within the ribosomal DNA of Drosophila melanogaster. J Mol Evol 1994, 39:151-159.
59. Lindner D.L., Banik M.T. Intragenomic variation in the ITS rDNA region obscures phylogenetic relationships and inflates estimates of operational taxonomic units in genus Laetiporus. Mycologia 2011, 103:731-740.
60. Lindner D.L., Carlsen T., Henrik Nilsson R., Davey M., Schumacher T., Kauserud H. Employing 454 amplicon pyrosequencing to reveal intragenomic divergence in the internal transcribed spacer rDNA region in fungi. Ecol Evol 2013, 3:1751-1764.
61. Liu H., Pan G., Luo B., Li T., Yang Q., Vossbrinck C.R., Debrunner-Vossbrinck B.A., Zhou Z. Intraspecific polymorphism of rDNA among five Nosema bombycis isolates from different geographic regions in China. J Invertebr Pathol 2013, 113:63-69.
62. Massana R., del Campo J., Sieracki M.E., Audic S., Logares R. Exploring the uncultured microeukaryote majority in the oceans: reevaluation of ribogroups within stramenopiles. ISME J 2014, 8:854-866.
63. Mayol M., Rosselló J.A. Why nuclear ribosomal DNA spacers (ITS) tell different stories in Quercus. Mol Phylogenet Evol 2001, 19:167-176.
64. Meyer C.P., Paulay G. DNA barcoding: Error rates based on comprehensive sampling. PLoS Biol 2005, 3:e422.
65. Michon A.-L., Aujoulat F., Roudière L., Soulier O., Zorgniotti I., Jumas-Bilak E., Marchandin H. Intragenomic and intraspecific heterogeneity in rrs may surpass interspecific variability in a natural population of Veillonella. Microbiology 2010, 156:2080-2091.
66. Miranda L.N., Zhuang Y., Zhang H., Lin S. Phylogenetic analysis guided by intragenomic SSU rDNA polymorphism refines classification of "Alexandrium tamarense" species complex. Harmful Algae 2012, 16:35-48.
67. Moniz M.B.J., Kaczmarska I. Barcoding of diatoms: Nuclear encoded ITS revisited. Protist 2010, 161:7-34.
68. Morandi A., Zhaxybayeva O., Gogarten J.P., Graf J. Evolutionary and diagnostic implications of intragenomic heterogeneity in the 16S rRNA gene in Aeromonas strains. J Bacteriol 2005, 187:6561-6564.
69. Moreira D., von der Heyden S., Bass D., López-García P., Chao E., Cavalier-Smith T. Global eukaryote phylogeny: Combined small- and large-subunit ribosomal DNA trees support monophyly of Rhizaria, Retaria and Excavata. Mol Phylogenet Evol 2007, 44:255-266.
70. Morgan M.J., Chariton A.A., Hartley D.M., Hardy C.M. Improved inference of taxonomic richness from environmental DNA. PloS ONE 2013, 8:e71974.
71. Nassonova E., Smirnov A., Fahrni J., Pawlowski J. Barcoding amoebae: comparison of SSU, ITS and COI genes as tools for molecular identification of naked lobose amoebae. Protist 2010, 161:102-115.
72. Nilsson R.H., Kristiansson E., Ryberg M., Hallenberg N., Larsson K.-H. Intraspecific ITS variability in the kingdom Fungi as expressed in the international sequence databases and its implications for molecular species identification. Evol Bioinform Online 2008, 4:193-201.
73. O'mahony E.M., Tay W.T., Paxton R.J. Multiple rRNA variants in a single spore of the microsporidian Nosema bombi. J Eukaryot Microbiol 2007, 54:103-109.
74. Orsini L., Procaccini G., Sarno D., Montresor M. Multiple rDNA ITS-types within the diatom Pseudo-nitzschia delicatissima (Bacillariophyceae) and their relative abundances across a spring bloom in the Gulf of Naples. Mar Ecol-Prog Ser 2004, 271:87-98.
75. Parfrey L.W., Lahr D.J.G., Katz L.A. The dynamic nature of eukaryotic genomes. Mol Biol Evol 2008, 25:787-794.
76. Parfrey L.W., Grant J., Katz L.A. Ribosomal DNA is differentially amplified across life-cycle stages in the foraminifer Allogromia laticollaris strain CSH. J Foram Res 2012, 42:151-155.
77. Pawlowski J., Lecroq B. Short rDNA barcodes for species identification in Foraminifera. J Eukaryot Microbiol 2010, 57:197-205.
78. Pawlowski J., Bolivar I., Fahrni J.F., Cavalier-Smith T., Gouy M. Early origin of foraminifera suggested by SSU rRNA gene sequences. Mol Biol Evol 1996, 13:445-450.
79. Pawlowski J., Bolivar I., Guiard-Maffia J., Gouy M. Phylogenetic position of foraminifera inferred from LSU rRNA gene sequences. Mol Biol Evol 1994, 11:929-938.
80. Pawlowski J., Bolivar I., Fahrni J.F., de Vargas C., Gouy M., Zaninetti L. Extreme differences in rates of molecular evolution of foraminifera revealed by comparison of ribosomal DNA sequences and the fossil record. Mol Biol Evol 1997, 14:498-505.
81. Pawlowski J., Fahrni J., Lecroq B., Longet D., Cornelius N., Excoffier L., Cedhagen T., Gooday A.J. Bipolar gene flow in deep-sea benthic foraminifera. Mol Ecol 2007, 16:4089-4096.
82. Pawlowski J., Audic S., Adl S., Bass D., Belbahri L., Berney C., Bowser S.S., Cepicka I., Decelle J., Dunthorn M., et al. CBOL Protist Working Group: Barcoding Eukaryotic Richness beyond the Animal, Plant, and Fungal Kingdoms. PLoS Biol 2012, 10:e1001419.
83. Peterson A., John H., Koch E., Peterson J. A molecular phylogeny of the genus Gagea (Liliaceae) in Germany inferred from non-coding chloroplast and nuclear DNA sequences. Plant Syst Evol 2004, 245:145-162.
84. Pillet L., Fontaine D., Pawlowski J. Intra-genomic ribosomal RNA polymorphism and morphological variation in Elphidium macellum suggests inter-specific Hybridization in Foraminifera. PLoS ONE 2012, 7:e32373.
85. Pillet L., de Vargas C., Pawlowski J. Molecular identification of sequestered diatom chloroplasts and kleptoplastidy in Foraminifera. Protist 2011, 162:394-404.
86. Rooney A.P. Mechanisms underlying the evolution and maintenance of functionally heterogeneous 18S rRNA genes in apicomplexans. Mol Biol Evol 2004, 21:1704-1711.
87. Ruggiero M.V., Procaccini G. The rDNA ITS region in the Lessepsian marine angiosperm Halophila stipulacea (Forssk.) Aschers. (Hydrocharitaceae): Intragenomic variability and putative pseudogenic sequences. J Mol Evol 2004, 58:115-121.
88. Schloss P.D., Gevers D., Westcott S.L. Reducing the effects of PCR amplification and sequencing artifacts on 16S rRNA-based studies. PloS ONE 2011, 6:e27310.
89. Schweizer M., Pawlowski J., Kouwenhoven T.J., Guiard J., Van der Zwaan B. Molecular phylogeny of Rotaliida (Foraminifera) based on complete small subunit rDNA sequences. Marine Micropaleontol 2008, 66:233-246.
90. Shibalev D.V., Voronov A.S., Firsov S.Y., Ryskov A.P., Kupriyanova N.S. Detection of intragenomic polymorphism of the LR2 region in the human ribosomal intergenic spacer. Mol Biol 2004, 38:835-838.
91. Simon U.K., Weiß M. Intragenomic variation of fungal ribosomal genes Is higher than previously thought. Mol Biol Evol 2008, 25:2251-2254.
92. Stoeck T., Przybos E., Dunthorn M. The D1-D2 region of the large subunit ribosomal DNA as barcode for ciliates. Mol Ecol Resour 2014, 14:458-468.
93. Stoeck T., Behnke A., Christen R., Amaral-Zettler L., Rodriguez-Mora M.J., Chistoserdov A., Orsi W., Edgcomb V.P. Massively parallel tag sequencing reveals the complexity of anaerobic marine protistan communities. BMC Biol 2009, 7:72.
94. Stoupin D., Kiss A.K., Arndt H., Shatilovich A.V., Gilichinsky D.A., Nitsche F. Cryptic diversity within the choanoflagellate morphospecies complex Codosiga botrytis - Phylogeny and morphology of ancient and modern isolates. Eur J Protistol 2012, 48:263-273.
95. Strachan T., Webb D., Dover G.A. Transition stages of molecular drive in multiple-copy DNA families in Drosophila. EMBO J 1985, 4:1701-1708.
96. Thornhill D.J., Lord J.B. Secondary structure models for the internal transcribed spacer (ITS) region 1 from symbiotic dinoflagellates. Protist 2010, 161:434-451.
97. Thornhill D.J., Lajeunesse T.C., Santos S.R. Measuring rDNA diversity in eukaryotic microbial systems: how intragenomic variation, pseudogenes, and PCR artifacts confound biodiversity estimates. Mol Ecol 2007, 16:5326-5340.
98. Vogler A.P., DeSalle R. Evolution and phylogenetic information content of the ITS-1 region in the tiger beetle Cicindela dorsalis. Mol Biol Evol 1994, 11:393-405.
99. Weber A.A.-T., Pawlowski J. Can abundance of protists be inferred from sequence data: A case study of Foraminifera. PLoS ONE 2013, 8:e56739.
100. Wendel J.F. Genome evolution in polyploids. Plant Mol Evol 2000, 42:225-249.
101. Wissemann V. Hybridization and the evolution of the nrITS spacer region. Plant Genome Biodivers Evol 2003, 1:57-71.
102. Woese C.R., Kandler O., Wheelis M.L. Towards a natural system of organisms: proposal for the domains Archaea, Bacteria, and Eucarya. Proc Natl Acad Sci USA 1990, 87:4576-4579.
103. Wylezich C., Nies G., Mylnikov A.P., Tautz D., Arndt H. An evaluation of the use of the LSU rRNA D1-D5 domain for DNA-based taxonomy of eukaryotic protists. Protist 2010, 161:342-352.
104. Xu J., Zhang Q., Xu X., Wang Z., Qi J. Intragenomic variability and pseudogenes of ribosomal DNA in Stone flounder Kareius bicoloratus. Mol Phylogenet Evol 2009, 52:157-166.
105. Zhu F., Massana R., Not F., Marie D., Vaulot D. Mapping of picoeucaryotes in marine ecosystems with quantitative PCR of the 18S rRNA gene. FEMS Microbiol Ecol 2005, 52:79-92.