Strand-specific community RNA-seq reveals prevalent and dynamic antisense transcription in human gut microbiota

Frontiers in Microbiology

Volumn 6, Issue SEP, 2015, Pages

  Bao, Guanhui ^a   Wang, Mingjie ^a   Doak, Thomas G ^b   Ye, Yuzhen ^a  

^a INDIANA UNIVERSITY   (United States)

^b INDIANA UNIVERSITY   (United States)

Author keywords

Antisense RNA; Human gut microbiota; Metagenome; Metatranscriptome; Transposases

Indexed keywords

ANTISENSE TRANSCRIPTION; ARTICLE; BACTERIAL GENETICS; BACTEROIDES; GENE EXPRESSION; GENE MAPPING; GENETIC ANALYSIS; INTESTINE FLORA; METAGENOMICS; MICROBIAL COMMUNITY; NONHUMAN; RNA SEQUENCE; SEQUENCE ANALYSIS; SEQUENCE HOMOLOGY; TRANSCRIPTOMICS;

EID: 84946746270     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2015.00896     Document Type: Article

References (39)

1. Beaume, M., Hernandez, D., Farinelli, L., Deluen, C., Linder, P., Gaspin, C., et al. (2010). Cartography of methicillin-resistant S. aureus transcripts: detection, orientation and temporal expression during growth phase and stress conditions. PLoS ONE 5:e10725. doi: 10.1371/journal.pone.0010725
2. Behrens, S., Widder, S., Mannala, G. K., Qing, X. X., Madhugiri, R., Kefer, N., et al. (2014). Ultra deep sequencing of Listeria monocytogenes sRNA transcriptome revealed new antisense RNAs. PLoS ONE 9:e83979. doi: 10.1371/journal.pone.0083979
3. Beiter, T., Reich, E., Williams, R. W., and Simon, P. (2009). Antisense transcription: a critical look in both directions. Cell. Mol. Life Sci. 66, 94-112. doi: 10.1007/s00018-008-8381-y
4. Berretta, J., and Morillon, A. (2009). Pervasive transcription constitutes a new level of eukaryotic genome regulation. EMBO Rep. 10, 973-982. doi: 10.1038/embor.2009.181
5. Bolger, A. M., Lohse, M., and Usadel, B. (2014). Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30, 2114-2120. doi: 10.1093/bioinformatics/btu170
6. Brantl, S. (2007). Regulatory mechanisms employed by cis-encoded antisense RNAs. Curr. Opin. Microbiol. 10, 102-109. doi: 10.1016/j.mib.2007.03.012
7. Coolen, M. J., and Orsi, W. D. (2015). The transcriptional response of microbial communities in thawing Alaskan permafrost soils. Front. Microbiol. 6:197. doi: 10.3389/fmicb.2015.00197
8. de Menezes, A., Clipson, N., and Doyle, E. (2012). Comparative metatranscriptomics reveals widespread community responses during phenanthrene degradation in soil. Environ. Microbiol. 14, 2577-2588. doi: 10.1111/j.1462-2920.2012.02781.x
9. Dornenburg, J. E., Devita, A. M., Palumbo, M. J., and Wade, J. T. (2010). Widespread antisense transcription in Escherichia coli. MBio 1, e00024-e00110. doi: 10.1128/mBio.00024-10
10. Franzosa, E. A., Morgan, X. C., Segata, N., Waldron, L., Reyes, J., Earl, A. M., et al. (2014). Relating the metatranscriptome and metagenome of the human gut. Proc. Natl. Acad. Sci. U.S.A. 111, E2329-E2338. doi: 10.1073/pnas.1319284111
11. Garber, M., Grabherr, M. G., Guttman, M., and Trapnell, C. (2011). Computational methods for transcriptome annotation and quantification using RNA-seq. Nat. Methods 8, 469-477. doi: 10.1038/nmeth.1613
12. Giannoukos, G., Ciulla, D. M., Huang, K., Haas, B. J., Izard, J., Levin, J. Z., et al. (2012). Efficient and robust RNA-seq process for cultured bacteria and complex community transcriptomes. Genome Biol. 13, R23. doi: 10.1186/gb-2012-13-3-r23
13. Green, P. J., Pines, O., and Inouye, M. (1986). The role of antisense RNA in gene regulation. Annu. Rev. Biochem. 55, 569-597. doi: 10.1146/annurev.bi.55.070186.003033
14. Haas, B. J., Chin, M., Nusbaum, C., Birren, B. W., and Livny, J. (2012). How deep is deep enough for RNA-Seq profiling of bacterial transcriptomes? BMC Genomics 13:734. doi: 10.1186/1471-2164-13-734
15. He, S., Wurtzel, O., Singh, K., Froula, J. L., Yilmaz, S., Tringe, S. G., et al. (2010). Validation of two ribosomal RNA removal methods for microbial metatranscriptomics. Nat. Methods 7, 807-812. doi: 10.1038/nmeth.1507
16. Human Microbiome Project Consortium. (2012a). A framework for human microbiome research. Nature 486, 215-221. doi: 10.1038/nature11209
17. Human Microbiome Project Consortium. (2012b). Structure, function and diversity of the healthy human microbiome. Nature 486, 207-214. doi: 10.1038/nature11234
18. Jens, G., and Wolfgang, R. H. (2011). cis-antisense RNA, another level of gene regulation in bacteria. Microbiol. Mol. Biol. Rev. 75, 286-300. doi: 10.1128/MMBR.00032-10
19. Jorth, P., Turner, K. H., Gumus, P., Nizam, N., Buduneli, N., and Whiteley, M. (2014). Metatranscriptomics of the human oral microbiome during health and disease. MBio 5, e01012-e01014. doi: 10.1128/mBio.01012-14
20. Lacatena, R. M., and Cesareni, G. (1981). Base pairing of RNA I with its complementary sequence in the primer precursor inhibits ColE1 replication. Nature 294, 623-626. doi: 10.1038/294623a0
21. Langmead, B., and Salzberg, S. L. (2012). Fast gapped-read alignment with Bowtie 2. Nat. Methods 9, 357-359. doi: 10.1038/nmeth.1923
22. Leimena, M. M., Ramiro-Garcia, J., Davids, M., Van Den Bogert, B., Smidt, H., Smid, E. J., et al. (2013). A comprehensive metatranscriptome analysis pipeline and its validation using human small intestine microbiota datasets. BMC Genomics 14:530. doi: 10.1186/1471-2164-14-530
23. Levin, J. Z., Yassour, M., Adiconis, X. A., Nusbaum, C., Thompson, D. A., Friedman, N., et al. (2010). Comprehensive comparative analysis of strand-specific RNA sequencing methods. Nat. Methods 7, 709-715. doi: 10.1038/nmeth.1491
24. Liao, Y., Smyth, G. K., and Shi, W. (2014). featureCounts: an efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics 30, 923-930. doi: 10.1093/bioinformatics/btt656
25. Mao, F., Dam, P., Chou, J., Olman, V., and Xu, Y. (2009). DOOR: a database for prokaryotic operons. Nucleic Acids Res. 37, D459-D463. doi: 10.1093/nar/gkn757
26. Mitschke, J., Georg, J., Scholz, I., Sharma, C. M., Dienst, D., Bantscheff, J., et al. (2011). An experimentally anchored map of transcriptional start sites in the model cyanobacterium Synechocystis sp. PCC6803. Proc. Natl. Acad. Sci. U.S.A. 108, 2124-2129. doi: 10.1073/pnas.1015154108
27. Nealson, K. H., and Venter, J. C. (2007). Metagenomics and the global ocean survey: what's in it for us, and why should we care? ISME J. 1, 185-187. doi: 10.1038/ismej.2007.43
28. Passalacqua, K. D., Varadarajan, A., Weist, C., Ondov, B. D., Byrd, B., Read, T. D., et al. (2012). Strand-specific RNA-seq reveals ordered patterns of sense and antisense transcription in Bacillus anthracis. PLoS ONE 7:e43350. doi: 10.1371/journal.pone.0043350
29. Qin, J., Li, R., Raes, J., Arumugam, M., Burgdorf, K. S., Manichanh, C., et al. (2010). A human gut microbial gene catalogue established by metagenomic sequencing. Nature 464, 59-65. doi: 10.1038/nature08821
30. Remmele, C. W., Xian, Y., Albrecht, M., Faulstich, M., Fraunholz, M., Heinrichs, E., et al. (2014). Transcriptional landscape and essential genes of Neisseria gonorrhoeae. Nucleic Acids Res. 42, 10579-10595. doi: 10.1093/nar/gku762
31. Rusch, D. B., Halpern, A. L., Sutton, G., Heidelberg, K. B., Williamson, S., Yooseph, S., et al. (2007). The sorcerer II global ocean sampling expedition: northwest Atlantic through eastern tropical Pacific. PLoS Biol. 5:e77. doi: 10.1371/journal.pbio.0050077
32. Sharma, C. M., Hoffmann, S., Darfeuille, F., Reignier, J., Findeiss, S., Sittka, A., et al. (2010). The primary transcriptome of the major human pathogen Helicobacter pylori. Nature 464, 250-255. doi: 10.1038/nature08756
33. Siegel, T. N., Hon, C. C., Zhang, Q., Lopez-Rubio, J. J., Scheidig-Benatar, C., Martins, R. M., et al. (2014). Strand-specific RNA-Seq reveals widespread and developmentally regulated transcription of natural antisense transcripts in Plasmodium falciparum. BMC Genomics 15:150. doi: 10.1186/1471-2164-15-150
34. Sigurgeirsson, B., Emanuelsson, O., and Lundeberg, J. (2014). Analysis of stranded information using an automated procedure for strand specific RNA sequencing. BMC Genomics 15:631. doi: 10.1186/1471-2164-15-631
35. Simons, R. W., and Kleckner, N. (1983). Translational control of IS10 transposition. Cell 34, 683-691. doi: 10.1016/0092-8674(83)90401-4
36. Tang, T. H., Polacek, N., Zywicki, M., Huber, H., Brugger, K., Garrett, R., et al. (2005). Identification of novel non-coding RNAs as potential antisense regulators in the archaeon Sulfolobus solfataricus. Mol. Microbiol. 55, 469-481. doi: 10.1111/j.1365-2958.2004.04428.x
37. Tatusov, R. L., Koonin, E. V., and Lipman, D. J. (1997). A genomic perspective on protein families. Science 278, 631-637. doi: 10.1126/science.278.5338.631
38. Thomason, M. K., and Storz, G. (2010). Bacterial antisense RNAs: how many are there, and what are they doing? Annu. Rev. Genet. 44, 167-188. doi: 10.1146/annurev-genet-102209-163523
39. Wang, M., Ye, Y., and Tang, H. (2012). A de Bruijn graph approach to the quantification of closely-related genomes in a microbial community. J. Comput. Biol. 19, 814-825. doi: 10.1089/cmb.2012.0058