Microorganisms often regulate their gene expression at the level of transcription and/or translation in response to solar radiation. In this review, we present the use of both transcriptomics and proteomics to advance knowledge in the field of bacterial response to damaging radiation. Those studies pertain to diverse application areas such as fundamental microbiology, water treatment, microbial ecology and astrobiology. Even though it has been demonstrated that mRNA abundance is not always consistent with the protein regulation, we present here an exhaustive review on how bacteria regulate their gene expression at both transcription and translation levels to enable biomarkers identification and comparison of gene regulation from one bacterial species to another.
References
[1]
Sinha, R.P.; H?der, D.P. UV-induced DNA damage and repair: A review. Photochem. Photobiol. Sci. 2002, 1, 225–236, doi:10.1039/b201230h.
[2]
Friedberg, E.C. DNA damage and repair. Nature 2003, 421, 436–440, doi:10.1038/nature01408.
[3]
Matallana-Surget, S.; Meador, J.A.; Joux, F.; Douki, T. Effect of the GC content of DNA on the distribution of UVB-induced bipyrimidine photoproducts. Photochem. Photobiol. Sci. 2008, 7, 794–801, doi:10.1039/b719929e.
Fimognari, C.; Sestili, P.; Lenzi, M.; Bucchini, A.; Cantelli-Forti, G.; Hrelia, P. RNA as a new target for toxic and protective agents. Mutat. Res. 2008, 648, 15–22, doi:10.1016/j.mrfmmm.2008.09.003.
[6]
Cadet, J.; Sage, E.; Douki, T. Ultraviolet radiation-mediated damage to cellular DNA. Mut. Res. 2005, 571, 3–17, doi:10.1016/j.mrfmmm.2004.09.012.
[7]
Dizdaroglu, M. Mechanisms of Free Radical Damage to DNA. In DNA & Free Radicals: Techniques, Mechanisms & Applications; Aruoma, O.I., Halliwell, B., Eds.; OICA International: Santa Lucia and London, UK, 1998; pp. 3–26.
[8]
Sonntag, V. The Chemical Basis of Radiation Biology; Taylor and Francis: New York, NY, USA, 1987.
[9]
Douki, T. The variety of UV-induced pyrimidine dimeric photoproducts in DNA as shown by chromatographic quantification methods. Photochem. Photobiol. Sci. 2013, doi:10.1039/ C3PP25451H.
[10]
Cooper, S. Checkpoints and restriction points in bacteria and eukaryotic cells. BioEssays 2006, 28, 1035–1039, doi:10.1002/bies.20475.
[11]
Aldsworth, T.G.; Sharman, R.L.; Dodd, C.E.R. Bacterial suicide through stress. Cell. Mol. Life Sci. 1999, 56, 378–383, doi:10.1007/s000180050439.
[12]
Daly, M.J.; Gaidamakova, E.K.; Matrosova, V.Y.; Vasilenko, A.; Zhai, M.; Leapman, R.D.; Lai, B.; Ravel, B.; Li, S.M.W.; Kemner, K.M.; et al. Protein oxidation implicated as the primary determinant of bacterial radioresistance. PLoS Biol. 2007, 5, e92, doi:10.1371/journal.pbio.0050092.
Sharma, C.M.; Hoffmann, S.; Darfeuille, F.; Reignier, J.; Findeiss, S.; Sittka, A.; Chabas, S.; Reiche, K.; Hackermüller, J.; Reinhardt, R.; et al. The primary transcriptome of the major human pathogen Helicobacter pylori. Nature 2010, 464, 250–255, doi:10.1038/nature08756.
[15]
Filiatrault, M.J.; Stodghill, P.V.; Bronstein, P.A.; Moll, S.; Lindeberg, M.; Grills, G.; Schweitzer, P.; Wang, W.; Schroth, G.P.; Luo, S.; et al. Transcriptome analysis of Pseudomonas syringae identifies new genes, noncoding RNAs, and antisense activity. J. Bacteriol. 2010, 192, 2359–2372, doi:10.1128/JB.01445-09.
[16]
Kogenaru, S.; Qing, Y.; Guo, Y.; Wang, N. RNA-seq and microarray complement each other in transcriptome profiling. BMC Genomics 2012, 13, e629, doi:10.1186/1471-2164-13-629.
[17]
Yuan, M.; Chen, M.; Zhang, W.; Lu, W.; Wang, J.; Yang, M.; Zhao, P.; Tang, R.; Li, X.; Hao, Y.; et al. Genome sequence and transcriptome analysis of the radioresistant bacterium Deinococcus gobiensis: Insights into the extreme environmental adaptations. PLoS One 2012, 7, e34458, doi:10.1371/journal.pone.0034458.
[18]
Fu, X.; Fu, N.; Guo, S.; Yan, Z.; Xu, Y.; Hu, H.; Menzel, C.; Chen, W.; Li, Y.; Zeng, R.; et al. Estimating accuracy of RNA-Seq and microarrays with proteomics. BMC Genomics 2009, 10, e161.
[19]
Van den Bergh, G.; Arckens, L. Fluorescent two-dimensional difference gel electrophoresis unveils the potential of gel-based proteomics. Curr. Opin. Biotechnol. 2004, 15, 38–43, doi:10.1016/j.copbio.2003.12.001.
[20]
Gygi, S.P.; Rist, B.; Gerber, S.A.; Turecek, F.; Gelb, M.H.; Aebersold, R. Quantitative analysis of complex protein mixtures using isotope-coded affinity tags. Nat. Biotechnol. 1999, 17, 994–999, doi:10.1038/13690.
[21]
Krijgsveld, J.; Ketting, R.F.; Mahmoudi, T.; Johansen, J.; Artal-Sanz, M.; Verrijzer, C.P.; Plasterk, R.H.A.; Heck, A.J.R. Metabolic labeling of C. elegans and D. melanogaster for quantitative proteomics. Nat. Biotechnol. 2003, 21, 927–931, doi:10.1038/nbt848.
[22]
Zhong, H.; Marcus, S.L.; Li, L. Two-dimensional mass spectra generated from the analysis of 15N-labeled and unlabeled peptides for efficient protein identification and de novo peptide sequencing. J. Proteome Res. 2004, 3, 1155–1163, doi:10.1021/pr049900v.
[23]
Leroy, B.; Rosier, C.; Erculisse, V.; Leys, N.; Mergeay, M.; Wattiez, R. Differential proteomic analysis using isotope-coded protein-labeling strategies: Comparison, improvements and application to simulated microgravity effect on Cupriavidus metallidurans CH34. Proteomics 2010, 10, 2281–2291, doi:10.1002/pmic.200900286.
[24]
Matallana-Surget, S.; Leroy, B.; Wattiez, R. Shotgun proteomics: Concept, key points and data mining. Exp. Rev. Proteomics 2010, 7, 5–7, doi:10.1586/epr.09.101.
Oda, Y.; Huang, K.; Cross, F.R.; Cowburn, D.; Chait, B.T. Accurate quantitation of protein expression and site-specific phosphorylation. Proc. Natl. Acad. Sci.USA 1999, 96, 6591–6596, doi:10.1073/pnas.96.12.6591.
[27]
Conrads, T.P.; Alving, K.; Veenstra, T.D.; Belov, M.E.; Anderson, G.A.; Anderson, D.J.; Lipton, M.S.; Pasa-Tolic, L.; Udseth, H.R.; Chrisler, W.B.; et al. Quantitative analysis of bacterial and mammalian proteomes using a combination of cysteine affinity tags and 15N-metabolic labeling. Anal. Chem. 2001, 73, 2132–2139, doi:10.1021/ac001487x.
[28]
Liu, Y.; Zhou, J.; Omelchenko, M.V.; Beliaev, A.S.; Venkateswaran, A.; Stair, J.; Wu, L.; Thompson, D.K.; Xu, D.; Rogozin, I.B.; et al. Transcriptome dynamics of Deinococcus radiodurans recovering from ionizing radiation. Proc. Natl. Acad. Sci. USA 2003, 100, 4191–4196, doi:10.1073/pnas.0630387100.
[29]
Tanaka, M.; Earl, A.M.; Howell, H.A.; Park, M.J.; Eisen, J.A.; Peterson, S.N.; Battista, J.R. Analysis of Deinococcus radiodurans’s transcriptional response to ionizing radiation and dessication reveals novel proteins that contribute to extreme radioresistance. Genetics 2004, 168, 21–33, doi:10.1534/genetics.104.029249.
[30]
Zhang, C.; Jianfeng, W.; Zhiguo, Z.; Nanjiao, Y.; Duohong, S.; Yuejin, H. Proteomic analysis of Deinococcus radiodurans recovering from gamma-radiation. Proteomics 2005, 5, 138–143, doi:10.1002/pmic.200300875.
[31]
Lipton, M.S.; Pa?a-Toli?, L.; Anderson, G.A.; Anderson, D.J.; Auberry, D.L.; Battista, J.R.; Daly, M.J.; Fredrickson, J.; Hixson, K.K.; Kostandarithes, H.; et al. Global analysis of the Deinococcus radiodurans proteome by using accurate mass tags. Proc. Natl. Acad. Sci. USA 2002, 99, 11049–11054, doi:10.1073/pnas.172170199.
[32]
Ehling-Schulz, M.; Schulz, S.; Wait, R.; G?rg, A.; Scherer, S. The UV-B stimulon of the terrestrial cyanobacterium Nostoc commune comprises early shock proteins and late acclimation proteins. Mol. Microbiol. 2002, 46, 827–843, doi:10.1046/j.1365-2958.2002.03209.x.
[33]
Groot, A.; Dulermo, R.; Ortet, P.; Blanchard, L.; Guérin, P.; Fernandez, B.; Vacherie, B.; Dossat, C.; Jolivet, E.; Siguier, P.; et al. Alliance of proteomics and genomics to unravel the specificities of Sahara bacterium Deinococcus deserti. PLoS Genet. 2009, 5, e1000434, doi:10.1371/journal.pgen.1000434.
[34]
Christie-Oleza, J.A.; Fernandez, B.; Nogales, B.; Bosch, R.; Armengaud, J. Proteomic insights into the lifestyle of an environmentally relevant marine bacterium. ISME J. 2012, 6, 124–135, doi:10.1038/ismej.2011.86.
[35]
Kolker, E.; Picone, A.F.; Galperin, M.Y.; Romine, M.F.; Higdon, R.; Makarova, K.S.; Kolker, N.; Anderson, G.A.; Qiu, X.; Auberry, K.J.; et al. Global profiling of Shewanella oneidensis MR-1: Expression of hypothetical genes and improved functional annotations. Proc. Natl. Acad. Sci.USA 2005, 102, 2099–2104, doi:10.1073/pnas.0409111102.
[36]
Qiu, X.; Sundin, G.W.; Wu, L.; Zhou, J.; Tiedje, J.M. Comparative analysis of differentially expressed genes in Shewanella oneidensis MR-1 following exposure to UVC, UVB, and UVA radiation. J. Bacteriol. 2005, 187, 3556–3564, doi:10.1128/JB.187.10.3556-3564.2005.
[37]
Qiu, X.; Daly, M.J.; Vasilenko, A.; Omelchenko, M.V.; Gaidamakova, E.K.; Wu, L.; Zhou, J.; Sundin, G.W.; Tiedje, J.M. Transcriptome analysis applied to survival of Shewanella oneidensis MR-1 exposed to ionizing radiation. J. Bacteriol. 2006, 188, 1199–1204, doi:10.1128/JB.188.3.1199-1204.2006.
[38]
Berney, M.; Weilenmann, H.U.; Ihssen, J.; Bassin, C.; Egli, T. Specific growth rate determines the sensitivity of Escherichia coli to thermal, UVA, and solar disinfection. Appl. Environ. Microbiol. 2006, 72, 2586–2593, doi:10.1128/AEM.72.4.2586-2593.2006.
[39]
Vaishampayan, P.A.; Rabbow, E.; Horneck, G.; Venkateswaran, K.J. Survival of Bacillus pumilus spores for a prolonged period of time in real space conditions. Astrobiology 2012, 12, 487–497, doi:10.1089/ast.2011.0738.
[40]
Mastroleo, F.; van Houdt, R.; Leroy, B.; Benotmane, M.A.; Janssen, A.; Mergeay, M.; Vanhavere, F.; Hendrickx, L.; Wattiez, R.; Leys, N. Experimental design and environmental parameters affect Rhodospirillum rubrum S1H response to space flight. ISME J. 2009, 3, 1402–1419, doi:10.1038/ismej.2009.74.
[41]
Steglich, C.; Futschik, M.; Rector, T.; Steen, R.; Chisholm, S.W. Genome-wide analysis of light sensing in Prochlorococcus. J.Bacteriol. 2006, 188, 7796–7806, doi:10.1128/JB.01097-06.
[42]
Pandhal, J.; Wright, P.C.; Biggs, C.A. A quantitative proteomic analysis of light adaptation in a globally significant marine cyanobacterium Prochlorococcus marinus MED4. J. Proteome Res. 2007, 6, 996–1005, doi:10.1021/pr060460c.
[43]
Hihara, Y.; Kamei, A.; Kanehisa, M.; Kaplan, A.; Ikeuchi, M. DNA microarray analysis of cyanobacterial gene expression during acclimation to high light. Plant Cell. 2001, 13, 793–806.
[44]
Huang, L.; McCluskey, M.P.; Ni, H.; LaRossa, R.A. Global gene expression profiles of the cyanobacterium Synechocystis sp. strain PCC 6803 in response to irradiation with UV-B and white light. J. Bacteriol. 2002, 184, 6845–6858, doi:10.1128/JB.184.24.6845-6858.2002.
[45]
Matallana-Surget, S.; Joux, F.; Wattiez, R.; Lebaron, P. Proteome analysis of the UVB resistant marine bacterium Photobacterium angustum S14. PLoS One 2012, 7, e42299, doi:10.1371/journal.pone.0042299.
[46]
Matallana-Surget, S.; Joux, F.; Raftery, M.J.; Cavicchioli, R. The response of the marine bacterium Sphingopyxis alaskensis to solar radiation assessed by quantitative proteomics. Environ. Microbiol. 2009, 11, 2660–2675, doi:10.1111/j.1462-2920.2009.01992.x.
[47]
Narumi, I.; Satoh, K.; Cui, S.; Funayama, T.; Kitayama, S.; Watanabe, H. PprA: A novel protein from Deinococcus radiodurans that stimulates DNA ligation. Mol. Microbiol. 2004, 54, 278–285, doi:10.1111/j.1365-2958.2004.04272.x.
[48]
Ansong, C.; Purvine, S.O.; Adkins, J.N.; Lipton, M.S.; Smith, R.D. Proteogenomics: Needs and roles to be filled by proteomics in genome annotation. Briefs Funct. Genomics Proteomics 2008, 7, 50–62, doi:10.1093/bfgp/eln010.
[49]
Daly, M.J.; Gaidamakova, E.K.; Matrosova, V.Y.; Vasilenko, A.; Zhai, M.; Venkateswaran, A.; Hess, M.; Omelchenko, M.V.; Kostandarithes, H.M.; Makarova, K.S.; et al. Accumulation of Mn(II) in Deinococcus radiodurans facilitates gamma-radiation resistance. Science 2004, 306, 1025–1028, doi:10.1126/science.1103185.
[50]
Heidelberg, J.F.; Paulsen, I.T.; Nelson, K.E.; Gaidos, R.J.; Nelson, W.C.; Read, T.D.; Eisen, J.A.; Seshadri, R.; Ward, N.; Methe, B.; et al. Genome sequence of the dissimilatory metal ion-reducing bacterium Shewanella oneidensis. Nat. Biotechnol. 2002, 20, 1118–1123, doi:10.1038/nbt749.
[51]
Santos, A.L.; Gomes, N.C.M.; Henriques, I.; Almeida, A.; Correia, A.; Cunha, A. Role of transition metals in UVB-induced damage to bacteria. Photochem. Photobiol. 2013, 89, 640–648, doi:10.1111/php.12049.
[52]
Hollaender, A. Effect of long ultraviolet and short visible radiation on Escherichia coli. J. Bacteriol. 1943, 46, 531–541.
[53]
Quillardet, P.; Rouffaud, M.A.; Bouige, P. DNA array analysis of gene expression in response to UV irradiation in Escherichia coli. Res. Microbiol. 2003, 154, 559–572, doi:10.1016/S0923-2508(03)00149-9.
[54]
Hendrickx, L.; de Wever, H.; Hermans, V.; Mastroleo, F.; Morin, N.; Wilmotte, A.; Janssen, P.; Mergeay, M. Microbial ecology of the closed artificial ecosystem MELiSSA (Micro-Ecological Life Support System Alternative): Reinventing and compartmentalizing the Earth’s food and oxygen regeneration system for long-haul space exploration missions. Res. Microbiol. 2006, 157, 77–86, doi:10.1016/j.resmic.2005.06.014.
[55]
Whitman, W.B.; Coleman, D.C.; Wiebe, W.J. Prokaryotes: The unseen majority. Proc. Natl. Acad. Sci. USA 1998, 95, 6578–6583, doi:10.1073/pnas.95.12.6578.
[56]
Tedetti, M.; Sempéré, R. Penetration of UV radiation in the marine environment: A review. Photochem. Photobiol. 2006, 82, 89–397.
[57]
Madronich, S.; McKenzie, R.L.; Bj?rn, L.O.; Caldwell, M.M. Changes in biologically active ultraviolet radiation reaching the Earth’s surface. J. Photochem. Photobiol. B 1998, 46, 5–19, doi:10.1016/S1011-1344(98)00182-1.
[58]
Mary, I.; Tu, C.J.; Grossman, A.; Vaulot, D. Effects of high light on transcripts of stress-associated genes for the cyanobacteria Synechocystis sp. PCC 6803 and Prochlorococcus MED4 and MIT9313. Microbiology 2004, 150, 1271–1281, doi:10.1099/mic.0.27014-0.
[59]
Chatgilialoglu, C.; Ferreri, C.; Torreggiani, A.; Salzano, A.M.; Renzone, G.; Scaloni, A. Radiation-induced reductive modifications of sulfur-containing amino acids within peptides and proteins. J. Proteomics 2011, 74, 2264–2273, doi:10.1016/j.jprot.2011.03.012.
[60]
Dalle-Donne, I.; Rossi, R.; Giustarini, D.; Milzani, A.; Colombo, R. Protein carbonyls groups as biomarkers of oxidative stress. Clin. Chim. Acta 2003, 329, 23–38, doi:10.1016/S0009-8981(03)00003-2.
[61]
Dukan, S.; Farewell, A.; Ballesteros, M.; Taddei, F.; Radman, M.; Nystr?m, T. Protein oxidation in response to increased transcriptional or translational errors. Proc. Natl. Acad. Sci. USA 2000, 97, 5746–5749, doi:10.1073/pnas.100422497.
[62]
Ballesteros, M.; Fredriksson, A.; Henriksson, J.; Nystr?m, T. Bacterial senescence: Protein oxidation in non-proliferating cells is dictated by the accuracy of the ribosomes. EMBO J. 2001, 20, 5280–5289, doi:10.1093/emboj/20.18.5280.
Grune, T.; Merker, K.; Sandig, G.; Davies, K.J. Selective degradation of oxidatively modified protein substrates by the proteasome. Biochem. Biophys. Res. Commun. 2003, 305, 709–718, doi:10.1016/S0006-291X(03)00809-X.
[65]
Grune, T.; Jung, T.; Merker, K.; Davies, K.J.A. Decreased proteolysis caused by protein aggregates, inclusion bodies, plaques, lipofuscin, ceroid, and “aggresomes” during oxidative stress, aging, and disease. Int. J. Biochem. Cell Biol. 2004, 36, 2519–2530, doi:10.1016/j.biocel.2004.04.020.
[66]
Levine, R.L. Oxidative modification of glutamine synthetase. I. Inactivation is due to loss of one histidine residue. J. Biol. Chem. 1983, 258, 11823–11827.
[67]
Levine, R.L. Carbonyl modified proteins in cellular regulation, aging, and disease. Free Radic.Biol. Med. 2002, 32, 790–796, doi:10.1016/S0891-5849(02)00765-7.
[68]
Requena, J.R.; Levine, R.L.; Stadtman, E.R. Recent advances in the analysis of oxidized proteins. Amino Acids 2003, 25, 221–226, doi:10.1007/s00726-003-0012-1.
[69]
Krisko, A.; Radman, M. Protein and death by radiation in Escherichia coli and Deinococcus radiodurans. Proc. Natl. Acad. Sci.USA 2010, 107, 14373–14377, doi:10.1073/pnas.1009312107.
[70]
Desnues, B.; Gregori, G.; Dukan, S.; Aguilaniu, H.; Nystr?m, T. Differential oxidative damage and expression of stress regulons in culturable and nonculturable cells of Escherichia coli. EMBO Rep. 2003, 4, 400–440, doi:10.1038/sj.embor.embor799.
[71]
Bosshard, F.; Riedel, K.; Schneider, T.; Geiser, C.; Bucheli, M.; Egli, T. Protein oxidation and aggregation in UVA-irradiated Escherichia coli cells as signs of accelerated cellular senescence. Environ. Microbiol. 2010, 12, 2931–2945, doi:10.1111/j.1462-2920.2010.02268.x.
[72]
Matallana-Surget, S.; Cavicchioli, R.; Fauconnier, C.; Wattiez, R.; Leroy, B.; Joux, F.; Raftery, M.J.; Lebaron, P. Shotgun redox proteomics: identification and quantitation of carbonylated proteins in the UVB resistant marine bacterium, Photobacterium angustum S14. PLoS One 2013, 8, e68112, doi:10.1371/journal.pone.0068112.
[73]
Tamarit, J.; Cabiscol, E.; Ros, J. Identification of the major oxidatively damaged proteins in Escherichia coli cells exposed to oxidative stress. J. Biol. Chem. 1998, 273, 3027–3032, doi:10.1074/jbc.273.5.3027.