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Investigation of the Role of cyaA/crp Genes of Escherichia coli in Metal Stress

Yıl 2021, Cilt: 11 Sayı: 1, 1 - 22, 30.06.2021
https://doi.org/10.37094/adyujsci.834522

Öz

Adenosine 3 ′, 5′-monophosphate (cAMP) is an important signaling molecule. CRP, the receptor protein of cAMP, acts as the 'main' regulator for transcription factors. The CRP-cAMP complex directly controls at least 500 promoters in Escherichia coli. In this study, the roles of cyaA and crp genes in E. coli BW25113 strain under metal stress were investigated. The minimal inhibition concentration (MIC) and minimal cidal concentration (MCC) of 5 different metals (Zn, Ni, Co, Cd and Cu) on Escherichia coli BW25113 wild type, cyaA and crp mutant cells were determined. In addition, the effect of these metals on the survival of E. coli cyaA / crp mutants was determined by growth and drop plate method. According to E. coli BW25113 wild type, cyaA mutant strain was observed sensitivity in all metals except copper, whereas resistance was observed in crp mutant strain only to zinc metal. The roles of the cyaA and crp genes in metal stress were confirmed by completing the genes on the plasmid. As a result, the roles of cyaA and crp genes in metal resistance were revealed in this study.

Destekleyen Kurum

Bilecik Şeyh Edebali University

Proje Numarası

016-02.BŞEÜ.04-02

Teşekkür

We would like to thank Bilecik Şeyh Edebali University for supporting our study with the BAP project number 2016-02.BŞEÜ.04-02.

Kaynakça

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  • [3] Chandrangsu, P., Rensing, C., Helmann, J.D., Metal homeostasis and resistance in bacteria, Nature Reviews Microbiology,15, 338-350, 2017.
  • [4] Gray, H.B., Ellis Jr., W.R. Electron transfer In Bioinorganic Chemistry. (Bertini, I., Gray, H.B., Lippard, S.J. &Valentine, J.S., eds.), University Science Books, Mill Valley, California., pp. 315-363, 1994.
  • [5] Shaivastave, A., Singh V., Jadon, S., Bhadauria, S., Heavy Metal Tolerance of Three Different Bacteria Isolated from Industrial Effluent, International Journal of Pharmaceutical Research and Bio-Science, 2, 137-47, 2013.
  • [6] Hohl, H., Varma, A., Soil: The Living Matrix, Soil Heavy Metals, 1-18, 2010.
  • [7] Sherameti I, Varma A., Heavy metal contamination of soils: monitoring and remediation. Springer, New York 2015.
  • [8] Dixit R., Wasiullah, Malaviya, D., Pandiyan, K., Singh U.B., Sahu A., Shukla R., Singh B.P., Rai J.P., Sharma P.K., Lade H., Paul, D., Bioremediation of Heavy Metals from Soil and Aquatic Environment: An Overview of Principles and Criteria of Fundamental Processes, Sustainability, 7(2), 2189-2212, 2015.
  • [9] Kılınç, K.N., Dönmez, G., Mikroorganizmalarda Ağır Metal Stresine Yanıtın Proteom Analizi ile Araştırılması, Elektronik Mikrobiyoloji Dergisi TR, 06, 27-33, 2008.
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  • [11] Palmer, L.D., Skaar, E.P., Transition metals and virulence in bacteria, Annual Review of Genetics, 50, 67-91, 2016.
  • [12] Macomber, L., Hausinger, R.P., Mechanisms of nickel toxicity in microorganisms, Metallomics, 3, 1153-1162, 2011.
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  • [34] Xue, J., Tan, B., Yang, S., Luo, M., Xia, H., Zhang, X., Zhou, X., Yang, X., Yang, R., Li, Y. et al., Influence of cAMP receptor protein (CRP) on bacterial virulence and transcriptional regulation of allS by CRP in Klebsiella pneumoniae, Gene, 593, 28-33, 2016.
  • [35] El Mouali, Y., Gaviria-Cantin, T., Sa´ nchez-Romero, M.A., Gibert M., Westermann A.J., Vogel, J., Balsalobre, C., CRP-cAMP mediates silencing of Salmonella virulence at the post-transcriptional level, PLoS Genetics, 14:e1007401. 2018.
  • [36] Manneh-Roussel, J., Haycocks, J.R.J., Magan, A., Perez-Soto, N., Voelz, K., Camilli, A., Krachler, A.M., Grainger, D.C., cAMP receptor protein controls vibrio cholerae gene expression in response to host colonization, mBio., 9, 2018.
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  • [40] Hoben, H.J., Somasegaran, P., Comparison of the pour, spread, and drop plate methods for enumeration of Rhizobium spp. in inoculants made from presterilized peat, Applied and Environmental Microbiology, 44, 1246-1247, 1982.
  • [41] Li, C., Li, Y., Ding, C., The Role of Copper Homeostasis at the Host-Pathogen Axis: From Bacteria to Fungi, International Journal of Molecular Sciences., 20(1), 175, 2019.
  • [42] Solioz, M., Copper homeostasis in gram-negative bacteria, In: Copper and Bacteria: Evolution, Homeostasis and Toxicity. Cham: Springer International Publishing, 49-80, 2018.
  • [43] Rademacher, C., Masepohl, B., Copper-responsive gene regulation in bacteria, Microbiology, 158(10), 2451-2464, 2012.
  • [44] Mouali, Y.E., Gaviria-Cantin, T., MarõÂa Antonia SaÂnchez-Romero, M.A., Gibert, M., Westermann, A.J., Jörg Vogel, J., Balsalobre, C., CRP-cAMP mediates silencing of Salmonella virulence at the post-transcriptional level, PLoS Genetics, 14(6), 2018.
  • [45] Amin, N., Peterkofsky A., A Dual Mechanism for Regulating cAMP Levels in Escherichia coli, Journal of Biological Chemistry., 270, 11803-11805, 1995.
  • [46] Iwasa Y., Yonemitsu, K., Miyamoto, A calcium-dependent cyclic nucleotide phosphodiesterase from Escherichia coli, FEBS Letters., 124, 207-209, 1981.
  • [47] Sun, H., Lu, X., Gao, P., The exploration of the antibacterial mechanism of Fe3+ against bacteria. Brazilian Journal of Microbiology 42(1), 410-414, 2011.
  • [48] Irving, H.M.N.H., Williams, R.J.P., The stability of transition-metal complexes, Journal of the Chemical Society, 3192-3210, 1953.
  • [49] Shin, J.H., Helmann, J.D., Molecular logic of the Zur-regulated zinc deprivation response in Bacillus subtilis, Nature Communications. 7, 9, 2016.
  • [50] Waldron, K.J., Robinson, N.J., How do bacterial cells ensure that metalloproteins get the correct metal?, Nature Reviews Microbiology, 7, 25-35, 2009.
  • [51] Outten, C.E., O’Halloran, T.V., Femtomolar sensitivity of metalloregulatory proteins controlling zinc homeostasis, Science 292, 2488-2492, 2001.
  • [52] Patzer, S.I., Hantke, K., The ZnuABC high-affinity zinc uptake system and its regulator Zur in Escherichia coli, Molecular Microbiology. 28, 1199-1210, 1998.
  • [53] Lucarelli, D., Vasil, M.L., Meyer-Klaucke, W., Pohl, E., The metal-dependent regulators FurA and FurB from Mycobacterium tuberculosis, International Journal of Molecular Sciences. 9, 1548-1560, 2008.
  • [54] Shin, J.H., Oh, S.Y., Kim, S.J., Roe, J.H., The zinc-responsive regulator Zur controls a zinc uptake system and some ribosomal proteins in Streptomyces coelicolor A3(2), Journal of Bacteriology. 189, 4070-4077, 2007.
  • [55] Gilston, B.A., Wang, S.N., Marcus, M.D., Canalizo-Hernandez, M.A., Swindell, E.P., Xue, Y. et al., Structural and mechanistic basis of zinc regulation across the E. coli Zur regulon, PLOS Biology. 12, 16, 2014.
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Yıl 2021, Cilt: 11 Sayı: 1, 1 - 22, 30.06.2021
https://doi.org/10.37094/adyujsci.834522

Öz

Proje Numarası

016-02.BŞEÜ.04-02

Kaynakça

  • [1] Waldron, K.J., Robinson, N.J., How do bacterial cells ensure that metalloproteins get the correct metal?, Nature Reviews Microbiology, 7, 25-35, 2009.
  • [2] Porcheron, G., Garénaux, A., Proulx, J., Sabri, M., Dozois, C.M., Iron, copper, zinc, and manganese transport and regulation in pathogenic Enterobacteria: correlations between strains, site of infection and the relative importance of the different metal transport systems for virulence, Frontiers in Cellular and Infection Microbiology, 3, 90, 2013.
  • [3] Chandrangsu, P., Rensing, C., Helmann, J.D., Metal homeostasis and resistance in bacteria, Nature Reviews Microbiology,15, 338-350, 2017.
  • [4] Gray, H.B., Ellis Jr., W.R. Electron transfer In Bioinorganic Chemistry. (Bertini, I., Gray, H.B., Lippard, S.J. &Valentine, J.S., eds.), University Science Books, Mill Valley, California., pp. 315-363, 1994.
  • [5] Shaivastave, A., Singh V., Jadon, S., Bhadauria, S., Heavy Metal Tolerance of Three Different Bacteria Isolated from Industrial Effluent, International Journal of Pharmaceutical Research and Bio-Science, 2, 137-47, 2013.
  • [6] Hohl, H., Varma, A., Soil: The Living Matrix, Soil Heavy Metals, 1-18, 2010.
  • [7] Sherameti I, Varma A., Heavy metal contamination of soils: monitoring and remediation. Springer, New York 2015.
  • [8] Dixit R., Wasiullah, Malaviya, D., Pandiyan, K., Singh U.B., Sahu A., Shukla R., Singh B.P., Rai J.P., Sharma P.K., Lade H., Paul, D., Bioremediation of Heavy Metals from Soil and Aquatic Environment: An Overview of Principles and Criteria of Fundamental Processes, Sustainability, 7(2), 2189-2212, 2015.
  • [9] Kılınç, K.N., Dönmez, G., Mikroorganizmalarda Ağır Metal Stresine Yanıtın Proteom Analizi ile Araştırılması, Elektronik Mikrobiyoloji Dergisi TR, 06, 27-33, 2008.
  • [10] Lemire, J.A., Harrison, J.J., Turner, R.J., Antimicrobial activity of metals: mechanisms, molecular targets and applications, Nature Reviews Microbiology, 11, 371-384. 2013.
  • [11] Palmer, L.D., Skaar, E.P., Transition metals and virulence in bacteria, Annual Review of Genetics, 50, 67-91, 2016.
  • [12] Macomber, L., Hausinger, R.P., Mechanisms of nickel toxicity in microorganisms, Metallomics, 3, 1153-1162, 2011.
  • [13] Baksh K.A., Zamble, D.B. Allosteric control of metal-responsive transcriptional regulators in bacteria, Journal of Biological Chemistry, 295(6), 1673-1684, 2019.
  • [14] Bruins, R.M., Kapil, S., Oehme W.F., Microbial Resistance to Metals in the Environment, Ecotoxicology and Environmental Safety, 45, 198-207. 2000.
  • [15] Capdevila, D.A., Edmonds, K.A., Giedroc, D.P. Metallochaperones and metalloregulation in bacteria, Essays Biochemistry. 61, 177-200, 2017.
  • [16] Foster, A.W., Osman, D., Robinson, N.J., Metal preferences and metalation, Journal of Biological Chemistry. 289, 28095–28103, 2014.
  • [17] O’Halloran, T.V. Transition metals in control of gene expression, Science, 261, 715-725, 1993.
  • [18] Mermod, M., Magnani, D., Solioz, M., Stoyanov, J.V. The copper- inducible ComR (YcfQ) repressor regulates expression of ComC (YcfR), which affects copper permeability of the outer membrane of Escherichia coli, BioMetals, 25, 33-43. 2012.
  • [19] Harrison, J.J., Turner, R.J., Ceri, H., Persister cells, the biofilm matrix and tolerance to metal cations in biofilm and planktonic Pseudomonas aeruginosa, Environmental Microbiology 7 (7), 981-994, 2005.
  • [20] Grass, G., Rensing, C., Genes involved in copper homeostasis in Escherichia coli, Journal of Bacteriology, 183, 2145-2147, 2001.
  • [21] Rensing, C., Grass, G., Escherichia coli mechanisms of copper homeostasis in a changing environment, FEMS Microbiology Reviews, 27, 197-213. 2003.
  • [22] Rensing, C., Mitra, B., Rosen, B.P., The zntA gene of Escherichia coli encodes a Zn(II)-translocating P-type ATPase, Proceedings of the National Academy of Sciences USA, 94, 14326-14331, 1997.
  • [23] Lee, C., Kuo, Y.L., The evolution of diffusion barriers in copper metallization, The Journal of The Minerals, 59, 44-49, 2008.
  • [25] Valencia, E.Y., Braz, V.S., Guzzo, C., Marques M.V., Two RND proteins involved in heavy metal efflux in Caulobacter crescentus belong to separate clusters within proteobacteria, BMC Microbiology, 13:79, 1471-2180, 2013.
  • [25] Higuchi, M., Ozaki, H., Matsui, M., Sonoike, K., A T-DNA insertion mutant of AtHMA1 gene encoding a Cu transporting ATPase in Arabidopsis thaliana has a defect in the water–water cycle of photosynthesis, Journal of Photochemistry and Photobiology B: Biology, 94 (3), 205-213, 2009.
  • [26] Nies, D.H., Efflux-mediated heavy metal resistance in prokaryotes, FEMS Microbiology Reviews, 27, 313-339, 2003.
  • [27] Chao, Y., Fu, D., Kinetic Study of the Antiport Mechanism of an Escherichia coli Zinc Transporter, ZitB, Journal of Biological Chemistry, 279(13), 12043-12050, 2004.
  • [28] Wei, Y., Fu, D., Selective metal binding to a membraneembedded aspartate in the Escherichia coli metal transporter YiiP (FieF), Journal of Biological Chemistry, 280, 33716-33724, 2005.
  • [29] Blanco, P., Hernando-Amado, S., Reales-Calderon, J., Corona, F., Lira, F., Alcalde-Rico, M., vd., Bacterial multidrug efflux pumps: much more than antibiotic resistance determinants, Microorganisms, 4 (1), 14, 2016.
  • [30] Sakamoto,Y., Furukawa, S., Ogihara, H., Yamasaki, M., Fosmidomycin Resistance in Adenylate Cyclase Deficient (cya) Mutants of Escherichia coli, Bioscience, Biotechnology, and Biochemistry, 67(9), 2030-2033, 2003.
  • [31] Botsford, L. J., Cyclic AMP in Prokaryotes, Microbiological Rewievs, 56(1), 100-122. 1992.
  • [32] Nosho, K., Fukushima, H., Asai, T., Masahiro Nishio, M., Takamaru, R., Kobayashi-Kirschvink, K.J., Ogawa,T., Hidaka, M., Masaki, H., cAMP-CRP acts as a key regulator for the viable but non-culturable state in Escherichia coli, Microbiology, 164, 410-419, 2018.
  • [33] Shimada, T., Fujita, N., Yamamoto, K., Ishihama, A., Novel roles of cAMP receptor protein (CRP) in regulation of transport and metabolism of carbon sources. PLoS One, 6:e20081. 2011.
  • [34] Xue, J., Tan, B., Yang, S., Luo, M., Xia, H., Zhang, X., Zhou, X., Yang, X., Yang, R., Li, Y. et al., Influence of cAMP receptor protein (CRP) on bacterial virulence and transcriptional regulation of allS by CRP in Klebsiella pneumoniae, Gene, 593, 28-33, 2016.
  • [35] El Mouali, Y., Gaviria-Cantin, T., Sa´ nchez-Romero, M.A., Gibert M., Westermann A.J., Vogel, J., Balsalobre, C., CRP-cAMP mediates silencing of Salmonella virulence at the post-transcriptional level, PLoS Genetics, 14:e1007401. 2018.
  • [36] Manneh-Roussel, J., Haycocks, J.R.J., Magan, A., Perez-Soto, N., Voelz, K., Camilli, A., Krachler, A.M., Grainger, D.C., cAMP receptor protein controls vibrio cholerae gene expression in response to host colonization, mBio., 9, 2018.
  • [37] McDonough, K.A., Rodriguez, A., The myriad roles of cyclic AMP in microbial pathogens: from signal to sword, Nature Reviews Microbiology, 10, 27-38, 2011. [38] Miller, D., The Generic Strategy Trap, Journal of Business Strategy, 13(1), 37-41, 1992.
  • [39] Wiegand, I., Hilpert, K., Hancock, R.E., Agar and broth dilution methods to determine the minimal inhibitory concentration (MIC) of antimicrobial substances, Nature Protocols., 3(2), 163-75, 2008.
  • [40] Hoben, H.J., Somasegaran, P., Comparison of the pour, spread, and drop plate methods for enumeration of Rhizobium spp. in inoculants made from presterilized peat, Applied and Environmental Microbiology, 44, 1246-1247, 1982.
  • [41] Li, C., Li, Y., Ding, C., The Role of Copper Homeostasis at the Host-Pathogen Axis: From Bacteria to Fungi, International Journal of Molecular Sciences., 20(1), 175, 2019.
  • [42] Solioz, M., Copper homeostasis in gram-negative bacteria, In: Copper and Bacteria: Evolution, Homeostasis and Toxicity. Cham: Springer International Publishing, 49-80, 2018.
  • [43] Rademacher, C., Masepohl, B., Copper-responsive gene regulation in bacteria, Microbiology, 158(10), 2451-2464, 2012.
  • [44] Mouali, Y.E., Gaviria-Cantin, T., MarõÂa Antonia SaÂnchez-Romero, M.A., Gibert, M., Westermann, A.J., Jörg Vogel, J., Balsalobre, C., CRP-cAMP mediates silencing of Salmonella virulence at the post-transcriptional level, PLoS Genetics, 14(6), 2018.
  • [45] Amin, N., Peterkofsky A., A Dual Mechanism for Regulating cAMP Levels in Escherichia coli, Journal of Biological Chemistry., 270, 11803-11805, 1995.
  • [46] Iwasa Y., Yonemitsu, K., Miyamoto, A calcium-dependent cyclic nucleotide phosphodiesterase from Escherichia coli, FEBS Letters., 124, 207-209, 1981.
  • [47] Sun, H., Lu, X., Gao, P., The exploration of the antibacterial mechanism of Fe3+ against bacteria. Brazilian Journal of Microbiology 42(1), 410-414, 2011.
  • [48] Irving, H.M.N.H., Williams, R.J.P., The stability of transition-metal complexes, Journal of the Chemical Society, 3192-3210, 1953.
  • [49] Shin, J.H., Helmann, J.D., Molecular logic of the Zur-regulated zinc deprivation response in Bacillus subtilis, Nature Communications. 7, 9, 2016.
  • [50] Waldron, K.J., Robinson, N.J., How do bacterial cells ensure that metalloproteins get the correct metal?, Nature Reviews Microbiology, 7, 25-35, 2009.
  • [51] Outten, C.E., O’Halloran, T.V., Femtomolar sensitivity of metalloregulatory proteins controlling zinc homeostasis, Science 292, 2488-2492, 2001.
  • [52] Patzer, S.I., Hantke, K., The ZnuABC high-affinity zinc uptake system and its regulator Zur in Escherichia coli, Molecular Microbiology. 28, 1199-1210, 1998.
  • [53] Lucarelli, D., Vasil, M.L., Meyer-Klaucke, W., Pohl, E., The metal-dependent regulators FurA and FurB from Mycobacterium tuberculosis, International Journal of Molecular Sciences. 9, 1548-1560, 2008.
  • [54] Shin, J.H., Oh, S.Y., Kim, S.J., Roe, J.H., The zinc-responsive regulator Zur controls a zinc uptake system and some ribosomal proteins in Streptomyces coelicolor A3(2), Journal of Bacteriology. 189, 4070-4077, 2007.
  • [55] Gilston, B.A., Wang, S.N., Marcus, M.D., Canalizo-Hernandez, M.A., Swindell, E.P., Xue, Y. et al., Structural and mechanistic basis of zinc regulation across the E. coli Zur regulon, PLOS Biology. 12, 16, 2014.
  • [56] Zhu, R.F., Song, Y.Q., Liu, H.P., Yang, Y.F., Wang, S.L., Yi, C.Q. et al. Allosteric histidine switch for regulation of intracellular zinc(II) fluctuation, Proceedings of the National Academy of Sciences. U.S.A. 114, 13661-13666, 2017.
  • [57] Guerra, A.J., Dann, C.E., Giedroc, D.P. Crystal structure of the zinc-dependent MarR family transcriptional regulator AdcR in the Zn(II)-bound state, Journal of the American Chemical Society. 133, 19614-19617, 2011.
  • [58] Sanson, M., Makthal, N., Flores, A.R., Olsen, R.J., Musser, J.M., Kumaraswami, M. Adhesin competence repressor (AdcR) from Streptococcus pyogenes controls adaptive responses to zinc limitation and contributes to virulence, Nucleic Acids Research. 43, 418-432, 2015.
  • [59] Morby, A.P., Turner, J.S., Huckle, J.W., Robinson, N.J., SmtB is a metal-dependent repressor of the cyanobacterial metallothionein gene smtA—identification of a Zn inhibited DNA-protein complex, Nucleic Acids Research. 21, 921-925, 1993.
  • [60] Kondrat, F.D.L., Kowald, G.R., Scarff, C.A., Scrivens, J.H., Blindauer, C.A. Resolution of a paradox by native mass spectrometry: facile occupation of all four metal binding sites in the dimeric zinc sensor SmtB, Chemical Communications, 49, 813-815, 2013.
  • [61] Thelwell, C., Robinson, N.J., Turner-Cavet, J.S., An SmtB-like repressor from Synechocystis PCC 6803 regulates a zinc exporter, Proceedings of the National Academy of Sciences , U.S.A. 95, 10728-10733, 1998.
  • [62] Arunkumar, A.I., Campanello, G.C., Giedroc, D.P. Solution structure of a paradigm ArsR family zinc sensor in the DNA-bound state, Proceedings of the National Academy of Sciences, U.S.A. 106, 18177-18182, 2009.
  • [63] Darcan, C., Kaygusuz, Ö., Aydın, E., Investigation of the role of RpoS in Escherichia coli againts Metals, Anadolu University Journal of Science and Technology C- Life Sciences and Biotechnology, 7(2), 105-121, 2018.
  • [64] Dong, T., Kirchhof, G.M., Schellhorn, H.E., RpoS regulation of gene expression during exponential growth of Escherichia coli K12, Molecular Genetics and Genomics, 279, 267-277, 2008.
  • [65] Macomber, L., Rensing, C., Imlay, J.A., Intracellular copper does not catalyze the formation of oxidative DNA damage in Escherichia coli, Journal of Bacteriology 189, 1616-1626, 2007.
  • [66] Troxell, B., Ye, M., Yang, Y., Carrasco, S.E., Lou, Y., Yanga, X.F., Manganese and Zinc Regulate Virulence Determinants in Borrelia burgdorferi, Infection and Immunity, 81(8), 2743-2752, 2013.
Toplam 65 adet kaynakça vardır.

Ayrıntılar

Birincil Dil İngilizce
Konular Yapısal Biyoloji
Bölüm Biyoloji
Yazarlar

Gülçin Çetin Kılıçaslan 0000-0002-9625-224X

Özge Kaygusuz 0000-0002-3652-4266

Önder İdil 0000-0003-1744-4006

Cihan Darcan 0000-0003-0205-3774

Proje Numarası 016-02.BŞEÜ.04-02
Yayımlanma Tarihi 30 Haziran 2021
Gönderilme Tarihi 2 Aralık 2020
Kabul Tarihi 5 Mart 2021
Yayımlandığı Sayı Yıl 2021 Cilt: 11 Sayı: 1

Kaynak Göster

APA Çetin Kılıçaslan, G., Kaygusuz, Ö., İdil, Ö., Darcan, C. (2021). Investigation of the Role of cyaA/crp Genes of Escherichia coli in Metal Stress. Adıyaman University Journal of Science, 11(1), 1-22. https://doi.org/10.37094/adyujsci.834522
AMA Çetin Kılıçaslan G, Kaygusuz Ö, İdil Ö, Darcan C. Investigation of the Role of cyaA/crp Genes of Escherichia coli in Metal Stress. ADYU J SCI. Haziran 2021;11(1):1-22. doi:10.37094/adyujsci.834522
Chicago Çetin Kılıçaslan, Gülçin, Özge Kaygusuz, Önder İdil, ve Cihan Darcan. “Investigation of the Role of cyaA/Crp Genes of Escherichia Coli in Metal Stress”. Adıyaman University Journal of Science 11, sy. 1 (Haziran 2021): 1-22. https://doi.org/10.37094/adyujsci.834522.
EndNote Çetin Kılıçaslan G, Kaygusuz Ö, İdil Ö, Darcan C (01 Haziran 2021) Investigation of the Role of cyaA/crp Genes of Escherichia coli in Metal Stress. Adıyaman University Journal of Science 11 1 1–22.
IEEE G. Çetin Kılıçaslan, Ö. Kaygusuz, Ö. İdil, ve C. Darcan, “Investigation of the Role of cyaA/crp Genes of Escherichia coli in Metal Stress”, ADYU J SCI, c. 11, sy. 1, ss. 1–22, 2021, doi: 10.37094/adyujsci.834522.
ISNAD Çetin Kılıçaslan, Gülçin vd. “Investigation of the Role of cyaA/Crp Genes of Escherichia Coli in Metal Stress”. Adıyaman University Journal of Science 11/1 (Haziran 2021), 1-22. https://doi.org/10.37094/adyujsci.834522.
JAMA Çetin Kılıçaslan G, Kaygusuz Ö, İdil Ö, Darcan C. Investigation of the Role of cyaA/crp Genes of Escherichia coli in Metal Stress. ADYU J SCI. 2021;11:1–22.
MLA Çetin Kılıçaslan, Gülçin vd. “Investigation of the Role of cyaA/Crp Genes of Escherichia Coli in Metal Stress”. Adıyaman University Journal of Science, c. 11, sy. 1, 2021, ss. 1-22, doi:10.37094/adyujsci.834522.
Vancouver Çetin Kılıçaslan G, Kaygusuz Ö, İdil Ö, Darcan C. Investigation of the Role of cyaA/crp Genes of Escherichia coli in Metal Stress. ADYU J SCI. 2021;11(1):1-22.

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