Reverse transcriptase genes are highly abundant and transcriptionally active in marine plankton assemblages

ISME Journal

Volumn 10, Issue 5, 2016, Pages 1134-1146

  Lescot, Magali ^a   Hingamp, Pascal ^a   Kojima, Kenji K ^b   Villar, Emilie ^a   Romac, Sarah ^c,d   Veluchamy, Alaguraj ^e,k   Boccara, Martine ^e   Jaillon, Olivier ^f,g,h   Iudicone, Daniele ⁱ   Bowler, Chris ^e   Wincker, Patrick ^f,g,h   Claverie, Jean Michel ^a   Ogata, Hiroyuki ^j  

^a CNRS Aix Marseille University   (France)

^b Genetic Information Research Institute   (United States)

^c STATION BIOLOGIQUE DE ROSCOFF   (France)

^d SORBONNE UNIVERSITÉ   (France)

^e PSL RESEARCH UNIVERSITY   (France)

^f CEA Fontenay aux Roses Bâtiment 61   (France)

^g UNIVERSITÉ D EVRY VAL D ESSONNE   (France)

^h CNRS   (France)

ⁱ STAZIONE ZOOLOGICA ANTON DOHRN   (Italy)

^j KYOTO UNIVERSITY   (Japan)

^k KING ABDULLAH UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Saudi Arabia)

more..

Author keywords

[No Author keywords available]

Indexed keywords

EUKARYOTE; GENETIC ANALYSIS; GENOME; MARINE ECOSYSTEM; PHYLOGENY; PLANKTON; PROKARYOTE; RELATIVE ABUNDANCE;

BACTERIA (MICROORGANISMS); EUKARYOTA; PROKARYOTA;

RETROPOSON; RNA DIRECTED DNA POLYMERASE; SEA WATER;

ENZYMOLOGY; EUKARYOTE; GENETIC TRANSCRIPTION; GENETICS; ISOLATION AND PURIFICATION; METABOLISM; METAGENOME; MICROBIOLOGY; PHYLOGENY; PLANKTON; PROKARYOTIC CELL; RETROPOSON; VIROLOGY;

EUKARYOTA; METAGENOME; PHYLOGENY; PLANKTON; PROKARYOTIC CELLS; RETROELEMENTS; RNA-DIRECTED DNA POLYMERASE; SEAWATER; TRANSCRIPTION, GENETIC;

EID: 84948397541     PISSN: 17517362     EISSN: 17517370     Source Type: Journal    
DOI: 10.1038/ismej.2015.192     Document Type: Article

References (84)

1. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. (1990). Basic local alignment search tool. J Mol Biol 215: 403-410.
2. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W et al. (1997). Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25: 3389-3402.
3. Antoine D, Morel A, Andre J. (1995). Algal pigment distribution and primary production in the eastern Mediterranean as derived from Coastal Zone Color Scanner observations. J Geophys Res 100: 16193-16209.
4. Arambula D, Wong W, Medhekar BA, Guo H, Gingery M, Czornyj E et al. (2013). Surface display of a massively variable lipoprotein by a Legionella diversity-generating retroelement. Proc Natl Acad Sci USA 110: 8212-8217.
5. Arkhipova IR, Pyatkov KI, Meselson M, Evgen'ev MB. (2003). Retroelements containing introns in diverse invertebrate taxa. Nat Genet 33: 123-124.
6. Armbrust EV, Berges JA, Bowler C, Green BR, Martinez D, Putnam NH et al. (2004). The genome of the diatom Thalassiosira pseudonana: ecology, evolution, and metabolism. Science 306: 79-86.
7. Arnosti C, Fuchs BM, Amann R, Passow U. (2012). Contrasting extracellular enzyme activities of particle-associated bacteria from distinct provinces of the North Atlantic Ocean. Front Microbiol 3: 425.
8. Aziz RK, Breitbart M, Edwards RA. (2010). Transposases are the most abundant, most ubiquitous genes in nature. Nucleic Acids Res 38: 4207-4217.
9. Bennetzen JL, Wang H. (2014). The contributions of transposable elements to the structure, function, and evolution of plant genomes. Annu Rev Plant Biol 65: 505-530.
10. Berland BR, Bonin DJ, Maestrini SY. (1980). Azote ou phosphore? Considerations sur le 'paradoxe nutrionnel' de la mer Mediterranee. Oceanol Acta 3: 135-142.
11. Blanc G, Duncan G, Agarkova I, Borodovsky M, Gurnon J, Kuo A et al. (2010). The Chlorella variabilis NC64A genome reveals adaptation to photosymbiosis, coevo-lution with viruses, and cryptic sex. Plant Cell 22, 2943-2955.
12. Blanc G, Agarkova I, Grimwood J, Kuo A, Brueggeman A, Dunigan DD et al. (2012). The genome of the polar eukaryotic microalga Coccomyxa subellipsoidea reveals traits of cold adaptation. Genome Biol 13: R39.
13. Bork P, Bowler C, de Vargas C, Gorsky G, Karsenti E, Wincker P. (2015). Tara Oceans. Tara Oceans studies plankton at planetary scale. Introduction. Science 348: 873.
14. Bowler C, Allen AE, Badger JH, Grimwood J, Jabbari K, Kuo A et al. (2008). The Phaeodactylum genome reveals the evolutionary history of diatom genomes. Nature 456: 239-244.
15. Bringaud F, Muller M, Cerqueira GC, Smith M, Rochette A, El-Sayed NM et al. (2007). Members of a large retro-poson family are determinants of post-transcriptional gene expression in Leishmania. PLoS Pathog 3: 1291-1307.
16. Bulman S, Candy JM, Fiers M, Lister R, Conner AJ, Eady CC. (2011). Genomics of biotrophic, plant-infecting plasmodiophorids using in vitro dual cultures. Protist 162: 449-461.
17. Carr M, Nelson M, Leadbeater BS, Baldauf SL. (2008). Three families of LTR retrotransposons are present in the genome of the choanoflagellate Monosiga brevi-collis. Protist 159: 579-590.
18. Casacuberta E, Gonzalez J. (2013). The impact of transposable elements in environmental adaptation. Mol Ecol 22: 1503-1517.
19. Chaffron S, D'Ovidio F, Sunagawa S, Acinas SG, Coelho LP, De Monte S et al. (2014a), Contextual biodiversity data of selected samples from the Tara Oceans Expedition (2009-2013).
20. Chaffron S, Guidi L, D'Ovidio F, Speich S, Audic S, De Monte S et al. (2014b), Contextual environmental data of selected samples from the Tara Oceans Expedition (2009-2013).
21. Choulet F, Alberti A, Theil S, Glover N, Barbe V, Daron J et al. (2014). Structural and functional partitioning of bread wheat chromosome 3B. Science 345: 1249721.
22. Collen J, Porcel B, Carre W, Ball SG, Chaparro C, Tonon T et al. (2013). Genome structure and metabolic features in the red seaweed Chondrus crispus shed light on evolution of the Archaeplastida. Proc Natl Acad Sci USA 110: 5247-5252.
23. D'Ortenzio F, Ribera d'Alcala M. (2009). On the trophic regimes of the Mediterranean Sea: a satellite analysis. Biogeosciences 6: 139-148.
24. Darriba D, Taboada GL, Doallo R, Posada D. (2011). ProtTest 3: fast selection of best-fit models of protein evolution. Bioinformatics 27: 1164-1165.
25. de Vargas C, Audic S, Henry N, Decelle J, Mahe F, Logares R et al. (2015). Ocean plankton. Eukaryotic plankton diversity in the sunlit ocean. Science 348: 1261605.
26. Dereeper A, Guignon V, Blanc G, Audic S, Buffet S, Chevenet F et al. (2008). Phylogeny.fr: robust phylo-genetic analysis for the non-specialist. Nucleic Acids Res 36: W465-W469.
27. Derelle E, Ferraz C, Rombauts S, Rouze P, Worden AZ, Robbens S et al. (2006). Genome analysis of the smallest free-living eukaryote Ostreococcus tauri unveils many unique features. Proc Natl Acad Sci USA 103: 11647-11652.
28. Doolittle WF, Sapienza C. (1980). Selfish genes, the phenotype paradigm and genome evolution. Nature 284: 601-603.
29. Dreyfus M, Regnier P. (2002). The poly(A) tail of mRNAs: bodyguard in eukaryotes, scavenger in bacteria. Cell 111: 611-613.
30. Dunlap KA, Palmarini M, Varela M, Burghardt RC, Hayashi K, Farmer JL et al. (2006). Endogenous retroviruses regulate periimplantation placental growth and differentiation. Proc Natl Acad Sci USA 103: 14390-14395.
31. Finn RD, Clements J, Eddy SR. (2011). HMMER web server: interactive sequence similarity searching. Nucleic Acids Res 39: W29-W37.
32. Frada MJ, Schatz D, Farstey V, Ossolinski JE, Sabanay H, Ben-Dor S et al. (2014). Zooplankton may serve as transmission vectors for viruses infecting algal blooms in the ocean. Curr Biol 24: 2592-2597.
33. Galagan JE, Calvo SE, Borkovich KA, Selker EU, Read ND, Jaffe D et al. (2003). The genome sequence of the filamentous fungus Neurospora crassa. Nature 422: 859-868.
34. Gifford WD, Pfaff SL, Macfarlan TS. (2013). Transposable elements as genetic regulatory substrates in early development. Trends Cell Biol 23: 218-226.
35. Gladyshev EA, Arkhipova IR. (2011). A widespread class of reverse transcriptase-related cellular genes. Proc Natl Acad Sci USA 108: 20311-20316.
36. Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O. (2010). New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 59: 307-321.
37. Hingamp P, Grimsley N, Acinas SG, Clerissi C, Subirana L, Poulain J et al. (2013). Exploring nucleo-cytoplasmic large DNA viruses in Tara Oceans microbial metagenomes. ISME J 7: 1678-1695.
38. Hua-Van A, Le Rouzic A, Boutin TS, Filee J, Capy P. (2011). The struggle for life of the genome's selfish architects. Biol Direct 6: 19.
39. Inouye K, Tanimoto S, Kamimoto M, Shimamoto T, Shimamoto T. (2011). Two novel retron elements are replaced with retron-Vc95 in Vibrio cholerae. Micro-biol Immunol 55: 510-513.
40. Jaillon P, Chica C, Novoa EM, Hingamp P, Pelletier E, Poulain J et al. (submitted). Marine plankton reveal a large unknown portion of the eukaryotic gene repertoire.
41. Jurka J, Kapitonov VV, Pavlicek A, Klonowski P, Kohany O, Walichiewicz J. (2005). Repbase Update, a database of eukaryotic repetitive elements. Cytogenet Genome Res 110: 462-467.
42. Kapitonov VV, Tempel S, Jurka J. (2009). Simple and fast classification of non-LTR retrotransposons based on phylogeny of their RT domain protein sequences. Gene 448: 207-213.
43. Karsenti E, Acinas SG, Bork P, Bowler C, De Vargas C, Raes J et al. (2011). A holistic approach to marine eco-systems biology. PLoS Biol 9: e1001177.
44. Keeling PJ, Burki F, Wilcox HM, Allam B, Allen EE, Amaral-Zettler LA et al. (2014). The Marine Microbial Eukaryote Transcriptome Sequencing Project (MMETSP): illuminating the functional diversity of eukaryotic life in the oceans through transcriptome sequencing. PLoS Biol 12: e1001889.
45. Khan H, Kozera C, Curtis BA, Bussey JT, Theophilou S, Bowman S et al. (2007). Retrotransposons and tandem repeat sequences in the nuclear genomes of cryptomonad algae. J Mol Evol 64: 223-236.
46. Kojima KK, Fujiwara H. (2005). An extraordinary retrotransposon family encoding dual endonucleases. Genome Res 15: 1106-1117.
47. Kojima KK, Kanehisa M. (2008). Systematic survey for novel types of prokaryotic retroelements based on gene neighborhood and protein architecture. Mol Biol Evol 25: 1395-1404.
48. Korf I. (2004). Gene finding in novel genomes. BMC Bioinformatics 5: 59.
49. Krom MD, Kress N, Brenner S, Gordon L. (1991). Phosphorous limitation of primary productivity in the Eastern Mediterranean Sea. Limnol Oceanogr 36: 424-432.
50. Labonte JM, Field EK, Lau M, Chivian D, Van Heerden E, Wommack KE et al. (2015). Single cell genomics indicates horizontal gene transfer and viral infections in a deep subsurface Firmicutes population. Front Microbiol 6: 349.
51. Lander ES, Linton LM, Birren B, Nusbaum C, Zody MC, Baldwin J et al. (2001). Initial sequencing and analysis of the human genome. Nature 409: 860-921.
52. Lima-Mendez G, Faust K, Henry N, Decelle J, Colin S, Carcillo F et al. (2015). Ocean plankton. Determinants of community structure in the global plankton inter-actome. Science 348: 1262073.
53. Llorens C, Futami R, Covelli L, Dominguez-Escriba L, Viu JM, Tamarit D et al. (2011). The Gypsy Database (GyDB) of mobile genetic elements: release 2.0. Nucleic Acids Res 39: D70-D74.
54. Lorenzi H, Thiagarajan M, Haas B, Wortman J, Hall N, Caler E. (2008). Genome wide survey, discovery and evolution of repetitive elements in three Entamoeba species. BMC Genomics 9: 595.
55. Luo R, Liu B, Xie Y, Li Z, Huang W, Yuan J et al. (2012). SOAPdenovo2: an empirically improved memory-efficient short-read de novo assembler. GigaScience 1: 18.
56. Majorek KA, Dunin-Horkawicz S, Steczkiewicz K, Muszewska A, Nowotny M, Ginalski K et al. (2014). The RNase H-like superfamily: new members, comparative structural analysis and evolutionary classification. Nucleic Acids Res 42: 4160-4179.
57. Marchler-Bauer A, Zheng C, Chitsaz F, Derbyshire MK, Geer LY, Geer RC et al. (2013). CDD: conserved domains and protein three-dimensional structure. Nucleic Acids Res 41: D348-D352.
58. Maumus F, Allen AE, Mhiri C, Hu H, Jabbari K, Vardi A et al. (2009). Potential impact of stress activated retrotransposons on genome evolution in a marine diatom. BMC Genomics 10: 624.
59. Medhekar B, Miller JF. (2007). Diversity-generating retro-elements. Curr Opin Microbiol 10: 388-395.
60. Miller JL, Le Coq J, Hodes A, Barbalat R, Miller JF, Ghosh P. (2008). Selective ligand recognition by a diversity-generating retroelement variable protein. PLoS Biol 6: e131.
61. Moreau H, Verhelst B, Couloux A, Derelle E, Rombauts S, Grimsley N et al. (2012). Gene functionalities and genome structure in Bathycoccus prasinos reflect cellular specializations at the base of the green lineage. Genome Biol 13: R74.
62. Noguchi H, Park J, Takagi T. (2006). MetaGene: prokaryotic gene finding from environmental genome shotgun sequences. Nucleic Acids Res 34: 5623-5630.
63. Oksanen J, Kindt R, Legendre P, O'Hara B, Stevens MHH, Oksanen MJ et al. (2007). The vegan package. Community ecology package.
64. Orgel LE, Crick FH. (1980). Selfish DNA: the ultimate parasite. Nature 284: 604-607.
65. Palenik B, Grimwood J, Aerts A, Rouze P, Salamov A, Putnam N et al. (2007). The tiny eukaryote Ostreo-coccus provides genomic insights into the paradox of plankton speciation. Proc Natl Acad Sci USA 104: 7705-7710.
66. Pesant S, Not F, Picheral M, Kandels-Lewis S, Le Bescot N, Gorsky G et al. (2015). Open science resources for the discovery and analysis of Tara Oceans data. Scientific data 2: 150023.
67. Piednoel M, Donnart T, Esnault C, Graca P, Higuet D, Bonnivard E. (2013). LTR-retrotransposons in R. exoculata and other crustaceans: the outstanding success of GalEa-like copia elements. PLoS One 8: e57675.
68. Rho M, Schaack S, Gao X, Kim S, Lynch M, Tang H. (2010). LTR retroelements in the genome of Daphnia pulex. BMC Genomics 11: 425.
69. Rice P, Longden I, Bleasby A. (2000). EMBOSS: the European Molecular Biology Open Software Suite. Trends Genet 16: 276-277.
70. Riordan JD, Dupuy AJ. (2013). Domesticated transposable element gene products in human cancer. Mob Genet Elements 3: e26693.
71. Schnable PS, Ware D, Fulton RS, Stein JC, Wei F, Pasternak S et al. (2009). The B73 maize genome: complexity, diversity, and dynamics. Science 326: 1112-1115.
72. Schulz MH, Zerbino DR, Vingron M, Birney E. (2012). Oases: robust de novo RNA-seq assembly across the dynamic range of expression levels. Bioinformatics 28: 1086-1092.
73. Simon DM, Zimmerly S. (2008). A diversity of unchar-acterized reverse transcriptases in bacteria. Nucleic Acids Res 36: 7219-7229.
74. Siokou-Frangou I, Christaki U, Mazzocchi MG, Montresor M, Ribera d'Alcalá M, Vaqué D et al. (2010). Plankton in the open Mediterranean Sea: a review. Biogeosciences 7: 1543-1586.
75. Siomi MC, Sato K, Pezic D, Aravin AA. (2011). PIWI-interacting small RNAs: the vanguard of genome defence. Nat Rev Mol Cell Biol 12: 246-258.
76. Slotkin RK, Martienssen R. (2007). Transposable elements and the epigenetic regulation of the genome. Nature Rev Genet 8: 272-285.
77. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. (2013). MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Mol Biol Evol 30: 2725-2729.
78. Tara Oceans Consortium, Coordinators; Tara Oceans Expedition, Participants. (2014). Registry of selected samples from the Tara Oceans Expedition (2009-2013).
79. Teneng I, Stribinskis V, Ramos KS. (2007). Context-specific regulation of LINE-1. Genes Cells 12: 1101-1110.
80. Toro N, Nisa-Martinez R. (2014). Comprehensive phyloge-netic analysis of bacterial reverse transcriptases. PLoS One 9: e114083.
81. Watanabe T, Nozawa T, Aikawa C, Amano A, Maruyama F, Nakagawa I. (2013). CRISPR regulation of intraspecies diversification by limiting IS transposition and intercellular recombination. Genome Biol Evol 5: 1099-1114.
82. Wicker T, Sabot F, Hua-Van A, Bennetzen JL, Capy P, Chalhoub B et al. (2007). A unified classification system for eukaryotic transposable elements. Nat Rev Genet 8: 973-982.
83. Wootton JC. (1994). Non-globular domains in protein sequences: automated segmentation using complexity measures. Comput Chem 18: 269-285.
84. Zerbino DR, Birney E. (2008). Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Res 18: 821-829.