Abstract
Streptomyces bacteria are abundant in soil environments, where they have an unusual multicellular life cycle that involves filamentous growth and spore formation. They also produce an extraordinary range of compounds known as specialized metabolites , and it is through these compounds that they interact with many of their terrestrial neighbours. Specialized metabolite production is subject to a wide range of regulatory inputs, and it is predicted that non-coding RNAs are amongst the many regulators governing metabolic output. RNA-sequencing experiments have revealed many non-coding RNAs expressed within specialized metabolic clusters of diverse Streptomyces species, with antisense RNAs featuring prominently. Here, we highlight a number of specialized metabolites whose gene clusters contain known non-coding RNAs, and consider possible roles for these RNA regulators in influencing Streptomyces interactions with other organisms in the environment.
Matthew J. Moody—Stephanie E. Jones, these two authors contributed equally to this work.
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References
Abrudan MI, Smakman F, Grimbergen AJ, Westhoff S, Miller EL, van Wezel GP, Rozen DE (2015) Socially mediated induction and suppression of antibiosis during bacterial coexistence. Proc Natl Acad Sci USA 112(35):11054–11059. doi:10.1073/pnas.1504076112
Arena JP, Liu KK, Paress PS, Cully DF (1991) Avermectin-sensitive chloride currents induced by Caenorhabditis elegans RNA in Xenopus oocytes. Mol Pharmacol 40(3):368–374
Arias AA, Lambert S, Martinet L, Adam D, Tenconi E, Hayette MP, Ongena M, Rigali S (2015) Growth of desferrioxamine-deficient Streptomyces mutants through xenosiderophore piracy of airborne fungal contaminations. FEMS Microbiol Ecol 91(7). doi:10.1093/femsec/fiv080
Barke J, Seipke RF, Gruschow S, Heavens D, Drou N, Bibb MJ, Goss RJ, Yu DW, Hutchings MI (2010) A mixed community of actinomycetes produce multiple antibiotics for the fungus farming ant Acromyrmex octospinosus. BMC Biol 8:109. doi:10.1186/1741-7007-8-109
Barona-Gomez F, Lautru S, Francou FX, Leblond P, Pernodet JL, Challis GL (2006) Multiple biosynthetic and uptake systems mediate siderophore-dependent iron acquisition in Streptomyces coelicolor A3(2) and Streptomyces ambofaciens ATCC 23877. Microbiology 152(Pt 11):3355–3366. doi:10.1099/mic.0.29161-0
Bentley SD, Chater KF, Cerdeno-Tarraga AM, Challis GL, Thomson NR, James KD, Harris DE, Quail MA, Kieser H, Harper D, Bateman A, Brown S, Chandra G, Chen CW, Collins M, Cronin A, Fraser A, Goble A, Hidalgo J, Hornsby T, Howarth S, Huang CH, Kieser T, Larke L, Murphy L, Oliver K, O’Neil S, Rabbinowitsch E, Rajandream MA, Rutherford K, Rutter S, Seeger K, Saunders D, Sharp S, Squares R, Squares S, Taylor K, Warren T, Wietzorrek A, Woodward J, Barrell BG, Parkhill J, Hopwood DA (2002) Complete genome sequence of the model actinomycete Streptomyces coelicolor A3(2). Nature 417(6885):141–147. doi:10.1038/417141a
Berendsen B, Pikkemaat M, Romkens P, Wegh R, van Sisseren M, Stolker L, Nielen M (2013) Occurrence of chloramphenicol in crops through natural production by bacteria in soil. J Agric Food Chem 61(17):4004–4010. doi:10.1021/jf400570c
Berry AM, Harriott OT, Moreau RA, Osman SF, Benson DR, Jones AD (1993) Hopanoid lipids compose the Frankia vesicle envelope, presumptive barrier of oxygen diffusion to nitrogenase. Proc Natl Acad Sci USA 90(13):6091–6094
Bibb MJ (2005) Regulation of secondary metabolism in streptomycetes. Curr Opin Microbiol 8(2):208–215. doi:10.1016/j.mib.2005.02.016
Bignell DR, Huguet-Tapia JC, Joshi MV, Pettis GS, Loria R (2010) What does it take to be a plant pathogen: genomic insights from Streptomyces species. Antonie Van Leeuwenhoek 98(2):179–194. doi:10.1007/s10482-010-9429-1
Broadbent D, Terry DA (1958) Effect of chloramphenicol on a fungus. Nature 182(4642):1107–1108
Cully DF, Paress PS, Liu KK, Schaeffer JM, Arena JP (1996) Identification of a Drosophila melanogaster glutamate-gated chloride channel sensitive to the antiparasitic agent avermectin. J Biol Chem 271(33):20187–20191
Currie CR, Scot JA, Summerbell RC, Malloch D (1999) Fungus-growing ants use antibiotic-producing bacteria to control garden parasites. Nature 398:701–704. doi:10.1038/19519
Davies J (2013) Specialized microbial metabolites: functions and origins. J Antibiot (Tokyo) 66(7):361–364. doi:10.1038/ja.2013.61
Fernandez-Martinez LT, Borsetto C, Gomez-Escribano JP, Bibb MJ, Al-Bassam MM, Chandra G (2014) New insights into chloramphenicol biosynthesis in Streptomyces venezuelae ATCC 10712. Antimicrob Agents Chemother 58(12):7441–7450. doi:10.1128/AAC.04272-14
Fernandez-Moreno MA, Caballero JL, Hopwood DA, Malpartida F (1991) The act cluster contains regulatory and antibiotic export genes, direct targets for translational control by the bldA tRNA gene of Streptomyces. Cell 66(4):769–780
Flärdh K, Buttner MJ (2009) Streptomyces morphogenetics: dissecting differentiation in a filamentous bacterium. Nat Rev Microbiol 7(1):36–49. doi:10.1038/nrmicro1968
Gao C, Hindra, Mulder D, Yin C, Elliot MA (2012) Crp is a global regulator of antibiotic production in S treptomyces. MBio 3(6). doi:10.1128/mBio.00407-12
Georg J, Hess WR (2011) cis-antisense RNA, another level of gene regulation in bacteria. Microbiol Mol Biol Rev 75(2):286–300. doi:10.1128/MMBR.00032-10
Ikeda H, Ishikawa J, Hanamoto A, Shinose M, Kikuchi H, Shiba T, Sakaki Y, Hattori M, Omura S (2003) Complete genome sequence and comparative analysis of the industrial microorganism Streptomyces avermitilis. Nat Biotechnol 21(5):526–531. doi:10.1038/nbt820
Jousselin A, Metzinger L, Felden B (2009) On the facultative requirement of the bacterial RNA chaperone. Hfq. Trends Microbiol 17(9):399–405. doi:10.1016/j.tim.2009.06.003
Kaltenpoth M, Gottler W, Herzner G, Strohm E (2005) Symbiotic bacteria protect wasp larvae from fungal infestation. Curr Biol 15(5):475–479. doi:10.1016/j.cub.2004.12.084
Kane NS, Hirschberg B, Qian S, Hunt D, Thomas B, Brochu R, Ludmerer SW, Zheng Y, Smith M, Arena JP, Cohen CJ, Schmatz D, Warmke J, Cully DF (2000) Drug-resistant Drosophila indicate glutamate-gated chloride channels are targets for the antiparasitics nodulisporic acid and ivermectin. Proc Natl Acad Sci USA 97(25):13949–13954. doi:10.1073/pnas.240464697
Kim MS, Dufour YS, Yoo JS, Cho YB, Park JH, Nam GB, Kim HM, Lee KL, Donohue TJ, Roe JH (2012) Conservation of thiol-oxidative stress responses regulated by SigR orthologues in actinomycetes. Mol Microbiol 85(2):326–344. doi:10.1111/j.1365-2958.2012.08115.x
Lautru S, Deeth RJ, Bailey LM, Challis GL (2005) Discovery of a new peptide natural product by Streptomyces coelicolor genome mining. Nat Chem Biol 1(5):265–269. doi:10.1038/nchembio731
Le TB, Fiedler HP, den Hengst CD, Ahn SK, Maxwell A, Buttner MJ (2009) Coupling of the biosynthesis and export of the DNA gyrase inhibitor simocyclinone in Streptomyces antibioticus. Mol Microbiol 72(6):1462–1474. doi:10.1111/j.1365-2958.2009.06735.x
Li CH, Cheng YW, Liao PL, Yang YT, Kang JJ (2010) Chloramphenicol causes mitochondrial stress, decreases ATP biosynthesis, induces matrix metalloproteinase-13 expression, and solid-tumor cell invasion. Toxicol Sci 116(1):140–150. doi:10.1093/toxsci/kfq085
Liu W, Sakr E, Schaeffer P, Talbot HM, Donisi J, Hartner T, Kannenberg E, Takano E, Rohmer M (2014) Ribosylhopane, a novel bacterial hopanoid, as precursor of C35 bacteriohopanepolyols in Streptomyces coelicolor A3(2). ChemBioChem 15(14):2156–2161. doi:10.1002/cbic.201402261
Luti KJ, Mavituna F (2011) Elicitation of Streptomyces coelicolor with dead cells of Bacillus subtilis and Staphylococcus aureus in a bioreactor increases production of undecylprodigiosin. Appl Microbiol Biotechnol 90(2):461–466. doi:10.1007/s00253-010-3032-2
Malott RJ, Steen-Kinnaird BR, Lee TD, Speert DP (2012) Identification of hopanoid biosynthesis genes involved in polymyxin resistance in Burkholderia multivorans. Antimicrob Agents Chemother 56(1):464–471. doi:10.1128/AAC.00602-11
McCormick JR, Flärdh K (2012) Signals and regulators that govern Streptomyces development. FEMS Microbiol Rev 36(1):206–231. doi:10.1111/j.1574-6976.2011.00317.x
McKenzie NL, Nodwell JR (2007) Phosphorylated AbsA2 negatively regulates antibiotic production in Streptomyces coelicolor through interactions with pathway-specific regulatory gene promoters. J Bacteriol 189(14):5284–5292. doi:10.1128/JB.00305-07
Meschke H, Walter S, Schrempf H (2012) Characterization and localization of prodiginines from Streptomyces lividans suppressing Verticillium dahliae in the absence or presence of Arabidopsis thaliana. Environ Microbiol 14(4):940–952. doi:10.1111/j.1462-2920.2011.02665.x
Montange RK, Batey RT (2008) Riboswitches: emerging themes in RNA structure and function. Annu Rev Biophys 37:117–133. doi:10.1146/annurev.biophys.37.032807.130000
Moody MJ, Young RA, Jones SE, Elliot MA (2013) Comparative analysis of non-coding RNAs in the antibiotic-producing Streptomyces bacteria. BMC Genom 14:558. doi:10.1186/1471-2164-14-558
Nett M, Ikeda H, Moore BS (2009) Genomic basis for natural product biosynthetic diversity in the actinomycetes. Nat Prod Rep 26(11):1362–1384. doi:10.1039/b817069j
Nitzan O, Suponitzky U, Kennes Y, Chazan B, Raul R, Colodner R (2010) Is chloramphenicol making a comeback? Isr Med Assoc J 12(6):371–374
Omura S, Crump A (2004) The life and times of ivermectin—a success story. Nat Rev Microbiol 2(12):984–989. doi:10.1038/nrmicro1048
Omura S, Ikeda H, Ishikawa J, Hanamoto A, Takahashi C, Shinose M, Takahashi Y, Horikawa H, Nakazawa H, Osonoe T, Kikuchi H, Shiba T, Sakaki Y, Hattori M (2001) Genome sequence of an industrial microorganism Streptomyces avermitilis: deducing the ability of producing secondary metabolites. Proc Natl Acad Sci USA 98(21):12215–12220. doi:10.1073/pnas.211433198
Onaka H, Mori Y, Igarashi Y, Furumai T (2011) Mycolic acid-containing bacteria induce natural-product biosynthesis in Streptomyces species. Appl Environ Microbiol 77(2):400–406. doi:10.1128/AEM.01337-10
Pan JJ, Solbiati JO, Ramamoorthy G, Hillerich BS, Seidel RD, Cronan JE, Almo SC, Poulter CD (2015) Biosynthesis of squalene from farnesyl diphosphate in bacteria: three steps catalyzed by three enzymes. ACS Cent Sci 1(2):77–82. doi:10.1021/acscentsci.5b00115
Perez J, Munoz-Dorado J, Brana AF, Shimkets LJ, Sevillano L, Santamaria RI (2011) Myxococcus xanthus induces actinorhodin overproduction and aerial mycelium formation by Streptomyces coelicolor. Microb Biotechnol 4(2):175–183. doi:10.1111/j.1751-7915.2010.00208.x
Poralla K, Muth G, Hartner T (2000) Hopanoids are formed during transition from substrate to aerial hyphae in Streptomyces coelicolor A3(2). FEMS Microbiol Lett 189(1):93–95
Rigali S, Titgemeyer F, Barends S, Mulder S, Thomae AW, Hopwood DA, van Wezel GP (2008) Feast or famine: the global regulator DasR links nutrient stress to antibiotic production by Streptomyces. EMBO Rep 9(7):670–675. doi:10.1038/embor.2008.83
Saenz JP, Sezgin E, Schwille P, Simons K (2012) Functional convergence of hopanoids and sterols in membrane ordering. Proc Natl Acad Sci USA 109(35):14236–14240. doi:10.1073/pnas.1212141109
Saha R, Saha N, Donofrio RS, Bestervelt LL (2013) Microbial siderophores: a mini review. J Basic Microbiol 53(4):303–317. doi:10.1002/jobm.201100552
Schmerk CL, Bernards MA, Valvano MA (2011) Hopanoid production is required for low-pH tolerance, antimicrobial resistance, and motility in Burkholderia cenocepacia. J Bacteriol 193(23):6712–6723. doi:10.1128/JB.05979-11
Schrempf H, Koebsch I, Walter S, Engelhardt H, Meschke H (2011) Extracellular Streptomyces vesicles: amphorae for survival and defence. Microb Biotechnol 4(2):286–299. doi:10.1111/j.1751-7915.2011.00251.x
Sciara G, Kendrew SG, Miele AE, Marsh NG, Federici L, Malatesta F, SchimpeRNA G, Savino C, Vallone B (2003) The structure of ActVA-Orf6, a novel type of monooxygenase involved in actinorhodin biosynthesis. EMBO J 22(2):205–215. doi:10.1093/emboj/cdg031
Seipke RF, Kaltenpoth M, Hutchings MI (2012) Streptomyces as symbionts: an emerging and widespread theme? FEMS Microbiol Rev 36(4):862–876. doi:10.1111/j.1574-6976.2011.00313.x
Swiercz JP, Hindra Bobek J, Haiser HJ, Di Berardo C, Tjaden B, Elliot MA (2008) Small non-coding RNAs in Streptomyces coelicolor. Nucleic Acids Res 36(22):7240–7251. doi:10.1093/nar/gkn898
Tahlan K, Ahn SK, Sing A, Bodnaruk TD, Willems AR, Davidson AR, Nodwell JR (2007) Initiation of actinorhodin export in Streptomyces coelicolor. Mol Microbiol 63(4):951–961
Traxler MF, Kolter R (2015) Natural products in soil microbe interactions and evolution. Nat Prod Rep 32(7):956–970. doi:10.1039/c5np00013k
Traxler MF, Seyedsayamdost MR, Clardy J, Kolter R (2012) Interspecies modulation of bacterial development through iron competition and siderophore piracy. Mol Microbiol 86(3):628–644. doi:10.1111/mmi.12008
Traxler MF, Watrous JD, Alexandrov T, Dorrestein PC, Kolter R (2013) Interspecies interactions stimulate diversification of the Streptomyces coelicolor secreted metabolome. MBio 4(4). doi:10.1128/mBio.00459-13
Uguru GC, Stephens KE, Stead JA, Towle JE, Baumberg S, McDowall KJ (2005) Transcriptional activation of the pathway-specific regulator of the actinorhodin biosynthetic genes in Streptomyces coelicolor. Mol Microbiol 58(1):131–150. doi:10.1111/j.1365-2958.2005.04817.x
Valton J, Mathevon C, Fontecave M, Niviere V, Ballou DP (2008) Mechanism and regulation of the two-component FMN-dependent monooxygenase ActVA-ActVB from Streptomyces coelicolor. J Biol Chem 283(16):10287–10296. doi:10.1074/jbc.M709730200
Vockenhuber MP, Sharma CM, Statt MG, Schmidt D, Xu Z, Dietrich S, Liesegang H, Mathews DH, Suess B (2011) Deep sequencing-based identification of small non-coding RNAs in Streptomyces coelicolor. RNA Biol 8(3):468–477
Wang R, Mast Y, Wang J, Zhang W, Zhao G, Wohlleben W, Lu Y, Jiang W (2013) Identification of two-component system AfsQ1/Q2 regulon and its cross-regulation with GlnR in Streptomyces coelicolor. Mol Microbiol 87(1):30–48. doi:10.1111/mmi.12080
Wang W, Ji J, Li X, Wang J, Li S, Pan G, Fan K, Yang K (2014) Angucyclines as signals modulate the behaviors of Streptomyces coelicolor. Proc Natl Acad Sci USA 111(15):5688–5693. doi:10.1073/pnas.1324253111
Waters LS, Storz G (2009) Regulatory RNAs in bacteria. Cell 136(4):615–628. doi:10.1016/j.cell.2009.01.043
Williamson NR, Fineran PC, Leeper FJ, Salmond GP (2006) The biosynthesis and regulation of bacterial prodiginines. Nat Rev Microbiol 4(12):887–899. doi:10.1038/nrmicro1531
Wu CH, Kong L, Bialecka-Fornal M, Park S, Thompson AL, Kulkarni G, Conway SJ, Newman DK (2015) Quantitative hopanoid analysis enables robust pattern detection and comparison between laboratories. Geobiology 13(4):391–407. doi:10.1111/gbi.12132
Xu G, Wang J, Wang L, Tian X, Yang H, Fan K, Yang K, Tan H (2010) “Pseudo” gamma-butyrolactone receptors respond to antibiotic signals to coordinate antibiotic biosynthesis. J Biol Chem 285(35):27440–27448. doi:10.1074/jbc.M110.143081
Xu Y, Willems A, Au-Yeung C, Tahlan K, Nodwell JR (2012) A two-step mechanism for the activation of actinorhodin export and resistance in Streptomyces coelicolor. MBio 3(5):e00191–00112. doi:10.1128/mBio.00191-12
Yang YL, Xu Y, Straight P, Dorrestein PC (2009) Translating metabolic exchange with imaging mass spectrometry. Nat Chem Biol 5(12):885–887. doi:10.1038/nchembio.252
Acknowledgments
This work was supported by an NSERC Discovery Grant (No. 04681), and an NSERC Discovery Accelerator Supplement. M.J.M. was supported by an NSERC Doctoral Scholarship, and S.E.J was supported by a Vanier Canada Graduate Scholarship.
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Moody, M.J., Jones, S.E., Crisante, D.A., Elliot, M.A. (2016). Streptomyces Bacteria: Specialized Metabolism, Inter-species Interations and Non-coding RNAs. In: Leitão, A., Enguita, F. (eds) Non-coding RNAs and Inter-kingdom Communication. Springer, Cham. https://doi.org/10.1007/978-3-319-39496-1_5
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