Metatranscriptomic analysis of microbes in an oceanfront deep-subsurface hot spring reveals novel small RNAs and type-specific tRNA degradation

Applied and Environmental Microbiology

Volumn 78, Issue 4, 2012, Pages 1015-1022

  Murakami, Shinnosuke ^a   Fujishima, Kosuke ^a   Tomita, Masaru ^a   Kanai, Akio ^a  

^a KEIO UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

16S RRNA GENE SEQUENCE; ANTICODONS; ARCHAEAL; BETAPROTEOBACTERIA; CDNA SEQUENCE; CULTURABLE; DEGRADATION STUDY; GLOBAL ENVIRONMENT; HOT SPRING WATER; NON-CODING RNAS; PHYLOGENETIC ANALYSIS; RICHMOND MINE; RNA SECONDARY STRUCTURES; SEQUENCE SIMILARITY; SMALL RNA; STREPTOMYCES COELICOLOR; UNDERGROUND ENVIRONMENT;

BACTERIA; BIOLOGY; DEGRADATION; ESCHERICHIA COLI; GROUNDWATER; HOT SPRINGS;

RNA;

ARCHAEAL RNA; BACTERIAL RNA; RNA 16S; TRANSFER RNA; UNTRANSLATED RNA;

META-ANALYSIS; OCEANIC FRONT; PH; PHYLOGENETICS; PROKARYOTE; RNA; THERMAL SPRING;

ARTICLE; CHEMISTRY; DNA SEQUENCE; GENETICS; HYDROTHERMAL VENT; JAPAN; METAGENOME; MICROBIOLOGY; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; RNA STABILITY;

HYDROTHERMAL VENTS; JAPAN; METAGENOME; MOLECULAR SEQUENCE DATA; RNA STABILITY; RNA, ARCHAEAL; RNA, BACTERIAL; RNA, RIBOSOMAL, 16S; RNA, TRANSFER; RNA, UNTRANSLATED; SEQUENCE ANALYSIS, DNA;

JAPAN;

ARCHAEA; BACTERIA (MICROORGANISMS); BETAPROTEOBACTERIA; ESCHERICHIA COLI; STREPTOMYCES COELICOLOR;

EID: 84857066577     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.06811-11     Document Type: Article

References (70)

1. Aiba H. 2007. Mechanism of RNA silencing by Hfq-binding small RNAs. Curr. Opin. Microbiol. 10:134-139.
2. Argaman L, et al. 2001. Novel small RNA-encoding genes in the intergenic regions of Escherichia coli. Curr. Biol. 11:941-950.
3. Arumugam M, et al. 2011. Enterotypes of the human gut microbiome. Nature 473:174-180.
4. Baker BJ, et al. 2010. Enigmatic, ultrasmall, uncultivated Archaea. Proc. Natl. Acad. Sci. U. S. A. 107:8806-8811.
5. Baker BJ, et al. 2006. Lineages of acidophilic archaea revealed by community genomic analysis. Science 314:1933-1935.
6. Barns SM, Fundyga RE, Jeffries MW, Pace NR. 1994. Remarkable archaeal diversity detected in a Yellowstone National Park hot spring environment. Proc. Natl. Acad. Sci. U. S. A. 91:1609-1613.
7. Bomar, L, Maltz M, Colston S, and Graf J. 2011. Directed culturing of microorganisms using metatranscriptomics. mBio 2:e00012-00011.
8. Buhler M, Spies N, Bartel DP, Moazed D. 2008. TRAMP-mediated RNA surveillance prevents spurious entry of RNAs into the Schizosaccharomyces pombe siRNA pathway. Nat. Struct. Mol. Biol. 15:1015-1023.
9. Chan PP, Lowe TM. 2009. GtRNAdb: a database of transfer RNA genes detected in genomic sequence. Nucleic Acids Res. 37:D93-D97.
10. Chen S, et al. 2002. A bioinformatics based approach to discover small RNA genes in the Escherichia coli genome. Biosystems 65:157-177.
11. Cole C, et al. 2009. Filtering of deep sequencing data reveals the existence of abundant Dicer-dependent small RNAs derived from tRNAs. RNA 15: 2147-2160.
12. Cole JR, et al. 2009. The Ribosomal Database Project: improved alignments and new tools for rRNA analysis. Nucleic Acids Res. 37:D141- D145.
13. Ding Y, Chan CY, Lawrence CE. 2005. RNA secondary structure prediction by centroids in a Boltzmann weighted ensemble. RNA 11:1157-1166.
14. Ding Y, Lawrence CE. 2003. A statistical sampling algorithm for RNA secondary structure prediction. Nucleic Acids Res. 31:7280-7301.
15. Emara MM, et al. 2010. Angiogenin-induced tRNA-derived stressinduced RNAs promote stress-induced stress granule assembly. J. Biol. Chem. 285:10959-10968.
16. Evguenieva-Hackenberg E. 2005. Bacterial ribosomal RNA in pieces. Mol. Microbiol. 57:318-325.
17. Gama-Castro S, et al. 2008. RegulonDB (version 6.0): gene regulation model of Escherichia coli K-12 beyond transcription, active (experimental) annotated promoters and Textpresso navigation. Nucleic Acids Res. 36:D120-D124.
18. Gantner S, Andersson AF, Alonso-Saez L, Bertilsson S. 2011. Novel primers for 16S rRNA-based archaeal community analyses in environmental samples. J. Microbiol. Methods 84:12-18.
19. Gardner PP, et al. 2009. Rfam: updates to the RNA families database. Nucleic Acids Res. 37:D136-D140.
20. Gottesman S. 2005. Micros for microbes: non-coding regulatory RNAs in bacteria. Trends Genet. 21:399-404.
21. Grice EA, et al. 2009. Topographical and temporal diversity of the human skin microbiome. Science 324:1190-1192.
22. Haiser HJ, Karginov FV, Hannon GJ, Elliot MA. 2008. Developmentally regulated cleavage of tRNAs in the bacterium Streptomyces coelicolor. Nucleic Acids Res. 36:732-741.
23. Hall JR, et al. 2008. Molecular characterization of the diversity and distribution of a thermal spring microbial community by using rRNA and metabolic genes. Appl. Environ. Microbiol. 74:4910-4922.
24. Inskeep WP, et al. 2010. Metagenomes from high-temperature chemotrophic systems reveal geochemical controls on microbial community structure and function. PLoS One 5:e9773.
25. Jost D, Nowojewski A, Levine E. 2011. Small RNA biology is systems biology. BMB Rep. 44:11-21.
26. Jurgens G, Saano A. 1999. Diversity of soil Archaea in boreal forest before, and after clear-cutting and prescribed burning. FEMS Microbiol. Ecol. 29:205-213.
27. Kato M, Chen X, Inukai S, Zhao H, Slack FJ. 2011. Age-associated changes in expression of small, noncoding RNAs, including microRNAs, in C. elegans. RNA 17:1804-1820.
28. Kawaji H, et al. 2008. Hidden layers of human small RNAs. BMC Genomics 9:157.
29. Kawano M, Reynolds AA, Miranda-Rios J, Storz G. 2005. Detection of 5'- and 3'-UTR-derived small RNAs and cis-encoded antisense RNAs in Escherichia coli. Nucleic Acids Res. 33:1040-1050.
30. Kvist T, Ahring BK, Westermann P. 2007. Archaeal diversity in Icelandic hot springs. FEMS Microbiol. Ecol. 59:71-80.
31. Larkin MA, et al. 2007. Clustal W and Clustal X version 2.0. Bioinformatics 23:2947-2948.
32. Lee YS, Shibata Y, Malhotra A, Dutta A. 2009. A novel class of small RNAs: tRNA-derived RNA fragments (tRFs). Genes Dev. 23:2639-2649.
33. Letunic I, Bork P. 2007. Interactive Tree Of Life (iTOL): an online tool for phylogenetic tree display and annotation. Bioinformatics 23:127-128.
34. Lowe TM, Eddy SR. 1997. tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res. 25: 955-964.
35. Marck C, Grosjean H. 2002. tRNomics: analysis of tRNA genes from 50 genomes of Eukarya, Archaea, and Bacteria reveals anticodon-sparing strategies and domain-specific features. RNA 8:1189-1232.
36. Masaki H, Ogawa T. 2002. The modes of action of colicins E5 and D, and related cytotoxic tRNases. Biochimie 84:433-438.
37. Massana R, Murray AE, Preston CM, DeLong EF. 1997. Vertical distribution and phylogenetic characterization of marine planktonic Archaea in the Santa Barbara Channel. Appl. Environ. Microbiol. 63:50-56.
38. Masse E, Escorcia FE, Gottesman S. 2003. Coupled degradation of a small regulatory RNA and its mRNA targets in Escherichia coli. Genes Dev. 17:2374-2383.
39. Milbury CA, Lee JC, Cannone JJ, Gaffney PM, Gutell RR. 2010. Fragmentation of the large subunit ribosomal RNA gene in oyster mitochondrial genomes. BMC Genomics 11:485.
40. Miyoshi T, Iwatsuki T, Naganuma T. 2005. Phylogenetic characterization of 16S rRNA gene clones from deep-groundwater microorganisms that pass through 0.2-micrometer-pore-size filters. Appl. Environ. Microbiol. 71:1084-1088.
41. Nunoura T, et al. 2005. Genetic and functional properties of uncultivated thermophilic crenarchaeotes from a subsurface gold mine as revealed by analysis of genome fragments. Environ. Microbiol. 7:1967-1984.
42. Nunoura T, et al. 2011. Insights into the evolution of Archaea and eukaryotic protein modifier systems revealed by the genome of a novel archaeal group. Nucleic Acids Res. 39:3204-3223.
43. Ogawa T, Inoue S, Yajima S, Hidaka M, Masaki H. 2006. Sequence-specific recognition of colicin E5, a tRNA-targeting ribonuclease. Nucleic Acids Res. 34:6065-6073.
44. Pruesse E, et al. 2007. SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Res. 35:7188-7196.
45. Raghavan R, Groisman EA, Ochman H. 2011. Genome-wide detection of novel regulatory RNAs in E. coli. Genome Res. 21:1487-1497.
46. Regalia M, Rosenblad MA, Samuelsson T. 2002. Prediction of signal recognition particle RNA genes. Nucleic Acids Res. 30:3368-3377.
47. Rivas E, Klein RJ, Jones TA, Eddy SR. 2001. Computational identification of noncoding RNAs in E. coli by comparative genomics. Curr. Biol. 11:1369-1373.
48. Schlax PJ, Xavier KA, Gluick TC, Draper DE. 2001. Translational repression of the Escherichia coli alpha operon mRNA: importance of an mRNA conformational switch and a ternary entrapment complex. J. Biol. Chem. 276:38494-38501.
49. Serganov A. 2009. The long and the short of riboswitches. Curr. Opin. Struct. Biol. 19:251-259.
50. Shi Y, Tyson GW, DeLong EF. 2009. Metatranscriptomics reveals unique microbial small RNAs in the ocean's water column. Nature 459:266-269.
51. Shinhara A, et al. 2011. Deep sequencing reveals as-yet-undiscovered small RNAs in Escherichia coli. BMC Genomics 12:428.
52. Szymanski M, Barciszewska MZ, Erdmann VA, Barciszewski J. 2002. 5S Ribosomal RNA Database. Nucleic Acids Res. 30:176-178.
53. Takai K, Horikoshi K. 1999. Genetic diversity of archaea in deep-sea hydrothermal vent environments. Genetics 152:1285-1297.
54. Takai K, Moser DP, DeFlaun M, Onstott TC, Fredrickson JK. 2001. Archaeal diversity in waters from deep South African gold mines. Appl. Environ. Microbiol. 67:5750-5760.
55. Tang TH, et al. 2002. RNomics in Archaea reveals a further link between splicing of archaeal introns and rRNA processing. Nucleic Acids Res. 30: 921-930.
56. Thompson DM, Lu C, Green PJ, Parker R. 2008. tRNA cleavage is a conserved response to oxidative stress in eukaryotes. RNA 14:2095-2103.
57. Thompson DM, Parker R. 2009. The RNase Rny1p cleaves tRNAs and promotes cell death during oxidative stress in Saccharomyces cerevisiae. J. Cell Biol. 185:43-50.
58. Tjaden B, et al. 2002. Transcriptome analysis of Escherichia coli using high-density oligonucleotide probe arrays. Nucleic Acids Res. 30:3732-3738.
59. Venter JC, et al. 2004. Environmental genome shotgun sequencing of the Sargasso Sea. Science 304:66-74.
60. Vogel J, et al. 2003. RNomics in Escherichia coli detects new sRNA species and indicates parallel transcriptional output in bacteria. Nucleic Acids Res. 31:6435-6443.
61. Warnecke F, Hess M. 2009. A perspective: metatranscriptomics as a tool for the discovery of novel biocatalysts. J. Biotechnol. 142:91-95.
62. Washietl S, Hofacker IL, Lukasser M, Huttenhofer A, Stadler PF. 2005. Mapping of conserved RNA secondary structures predicts thousands of functional noncoding RNAs in the human genome. Nat. Biotechnol. 23: 1383-1390.
63. Wassarman KM, Storz G. 2000. 6S RNA regulates E. coli RNA polymerase activity. Cell 101:613-623.
64. Weinberg Z, Perreault J, Meyer MM, Breaker RR. 2009. Exceptional structured noncoding RNAs revealed by bacterial metagenome analysis. Nature 462:656-659.
65. Weinberg Z, et al. 2010. Comparative genomics reveals 104 candidate structured RNAs from bacteria, archaea, and their metagenomes. Genome Biol. 11:R31.
66. Wilms R, et al. 2006. Specific bacterial, archaeal, and eukaryotic communities in tidal-flat sediments along a vertical profile of several meters. Appl. Environ. Microbiol. 72:2756-2764.
67. Winkler W, Nahvi A, Breaker RR. 2002. Thiamine derivatives bind messenger RNAs directly to regulate bacterial gene expression. Nature 419:952-956.
68. Xie W, et al. 2011. Comparative metagenomics of microbial communities inhabiting deep-sea hydrothermal vent chimneys with contrasting chemistries. ISME J. 5:414-426.
69. Yachie N, Numata K, Saito R, Kanai A, Tomita M. 2006. Prediction of non-coding and antisense RNA genes in Escherichia coli with gapped Markov model. Gene 372:171-181.
70. Zhang A, et al. 2003. Global analysis of small RNA and mRNA targets of Hfq. Mol. Microbiol. 50:1111-1124.