Bacillus subtilis Standart Suş (PY79) ile Basilisinin Bloke Edildiği Suşun (OGU1) Karşılaştırmalı Dinamik Sekretom Analizi

ÖZCENGİZ, Gülay; İŞLEREL, Elif Tekin

Bacillus subtilis Standart Suş (PY79) ile Basilisinin Bloke Edildiği Suşun (OGU1) Karşılaştırmalı Dinamik Sekretom Analizi

Yürütücü

Gülay ÖZCENGİZ (Orta Doğu Teknik Üniversitesi, Fen Bilimleri Enstitüsü, Biyoloji Bölümü, Ankara, Türkiye)

Araştırmacı(lar)

Elif Tekin İŞLEREL (Orta Doğu Teknik Üniversitesi, Fen Bilimleri Enstitüsü, Biyoloji Bölümü, Ankara, Türkiye)

3 4

Proje Grubu: KBAG Sayfa Sayısı: 80 Proje No: 116Z351 Proje Bitiş Tarihi: 15.08.2018 Metin Dili: Türkçe İndeks Tarihi: 16-01-2020

Bacillus subtilis Standart Suş (PY79) ile Basilisinin Bloke Edildiği Suşun (OGU1) Karşılaştırmalı Dinamik Sekretom Analizi

Öz:

Bacillus türleri, antimetabolik ve farmakolojik aktiviteye sahip çok çeşitli ikincil metabolitler üretmektedir. B. subtilis?e ait biyoaktif peptidlerin etkilerinin sadece antimikrobiyal aktivite ile sınırlı olmadığı bilinmektedir. B. subtilis tarafından üretilen basilisin, N-terminalinde L-alanine and C-terminalinde non-proteinojenik bir amino asit olan L-anticapsin?den oluşan dipeptid yapısı ile bilinen en küçük antibiyotiktir. Basilisin biyosentezinin dinamikleri ve moleküler regülasyonu ile ilgili literatür bilgilerinin çoğu grubumuz tarafından rapor edilmiştir. Biyosentezin hücre yoğunluğu sinyali global kontrol mekanizmasının bir parçası olduğu, transpozon mutajenez kütüphanesinin taranmasıyla gen düzeyinde anlaşılmış ve bu[Spo0K (Opp)?ye dayalı regülasyon ağı içerisinde ComQ/ComX, PhrC (CSF), ComP/ComA elementleri] ve transkripsiyon faktörler ComA, Spo0A, AbrB ve CodY?nin bac operonu üzerine etkileri, transkripsiyonal füzyon ve EMSA analizleri ile tarafımızca doğrulanmıştır. Önceki araştırmalarımızda basilisin üreticisi standart suş PY79 ve bunun basilisin operonunu bloke ederek oluşturduğumuz derivatifi OGU1?a ait sitozolik proteomların oldukça detaylı bir analizi yapılmıştır. Bu çalışmada, jele dayalı ve jelden bağımsız iki ayrı yaklaşım kullanılarak sekretom analizi ve bu suretle ulaşılabilen proteinlerin sayısının arttırılmasıyla B. subtilis?de basilisin üretimi yokluğunda ortaya çıkan sekretom değişimlerinin zaman ve mekan olarak dinamik bir analizi amaçlanmıştır. Kültivasyonun 12., 16. ve 24. saatlerinde mevcut sekretom bileşenleri tanımlanmış ve PY79 ve basilisin üretemeyen türevi OGU1 arasında farklılık gösteren proteinler ve seviyeleri nicel olarak belirlenmiştir. LC-MS/MS analizlerinde toplam 2075 protein tanımlanabilmiştir. Tanımlanabilen proteinlerin 166?sının iki suş arasında farklı ifade edilen proteinler olduğu gösterilmiştir. Beklenildiği üzere, 2DE MALDI TOF/MS yaklaşımı ile elde edilen protein sayıları çok daha düşük olmuşsa da, sonuçlar LC-MS/MS analiz bulguları ile uyumludur. Yine seçilen genler özelinde gerçekleştirilen qRT PCR çalışmaları da proteomik bulguları çok büyük ölçüde desteklemiştir. Bütünüyle ele alındığında, OGU1?de farklı ifade edilen proteinlerin transport ve metabolizma, genetik prosesler, yaşam biçimi, strese uyum, sporulasyon ve jerminasyon gibi fonksiyonal kategorilere ait olduğu gösterilmiştir. Çalışmamız, basilisin yokluğunda sekretom kompozisyonundaki değişimlerin kapsamlı biçimde anlaşılmasını ve bu değişimlerde basilisin operonunun muhtemel rolünün değerlendirilmesi gerekliliğine işaret etmiş olup mevcut bulguların daha ileri fonksiyonel çalışmalarla desteklenmesi hedeflenmektedir.

Anahtar Kelime: qRT PCR 2DE MALDI TOF/MS LC-MS/MS sekretom proteom basilisin Bacillus subtilis

Konular: Biyoloji Biyoteknoloji ve Uygulamalı Mikrobiyoloji

Erişim Türü: Erişime Açık

Abhyankar, W., Beek, A. T., Dekker, H., Kort, R., Brul, S., and de Koster, C. G. (2011). Gel‐free proteomic identification of the Bacillus subtilis insoluble spore coat protein fraction. Proteomics, 11(23), 4541-4550.
Dynamic comparative secretome analysis of Bacillus subtilis PY79 and its bacilysin blocked mutant (Bildiri - Uluslararası Bildiri - Poster Sunum)
Aebersold, R. and Mann, M. (2003). Mass spectrometry-based proteomics. Nature, 422(6928), 198-207.
Allenby NE, O'Connor N, Prágai Z, Ward AC, Wipat A, Harwood CR (2005) Genome-wide transcriptional analysis of the phosphate starvation stimulon of Bacillus subtilis. J Bacteriol. 187:8063-8080.
Antelmann, H., Darmon, E., Noone, D., Veening, J. W., Westers, H., Bron, S., Van Dijl, J. M. 2003. “The extracellular proteome of Bacillus subtilis under secretion stress conditions”, Molecular Microbiology, 49(1), 143-156.
Antelmann, H., Scharf, C., Hecker, M. 2000. “Phosphate starvation inducible proteins of Bacillus subtilis: proteomics and transcriptional analysis”, Journal of Bacteriolgy, 182, 4478-4490.
Antelmann, H., Tjalsma, H., Voigt, B., Ohlmeier, S., Bron, S., van Dijl, J. M., Hecker, M. 2001. “A proteomic view on genome- based signal peptide predictions”, Genome Research, 11(9), 1484-1502.
Antelmann, H., Töwe, S., Albrecht, D., Hecker, M. 2007. “The Phosphorus Source Phytate Changes the Composition of the Cell Wall Proteome in Bacillus subtilis”, Journal of Proteome Research, 6(2), 897-903.
Arocho, A., Chen, B., Ladanyi, M., & Pan, Q. (2006). Validation of the 2-ΔΔCt calculation as an alternate method of data analysis for quantitative PCR of BCR-ABL P210 transcripts. Diagnostic Molecular Pathology, 15(1), 56-61.
Atalla, A., and Schumann, W. (2003). “The pst operon of Bacillus subtilis is specifically induced by alkali stress”. Journal of Bacteriology, 185(16), 5019-5022.
Au N, Kuester-Schoeck E, Mandava V, Bothwell LE, Canny SP, Chachu K, Colavito SA, Fuller SN, Groban ES, Hensley LA, O'Brien TC, Shah A, Tierney JT, Tomm LL, O'Gara TM, Goranov AI, Grossman AD, O'brien TC (2005) Genetic composition of the Bacillus subtilis SOS system. J Bacteriol. 187:7655-7666.
Ball, M. S., & Karuso, P. (2007). Mass spectral compatibility of four proteomics stains. Journal of Proteome Research, 6(11), 4313-4320.
Banse AV, Chastanet A, Rahn-Lee L, Hobbs EC, Losick R (2008) Parallel pathways of repression and antirepression governing the transition to stationary phase in Bacillus subtilis. Proc Natl Acad Sci 105:15547-15552.
Barbe, V., Cruveiller, S., Kunst, F., Lenoble, P., Meurice, G., Sekowska, A., Danchin, A. 2009. “From a consortium sequence to a unified sequence: The Bacillus subtilis 168 reference genome a decade later”, Microbiology, 155, 1758-1775.
Barbieri, G., Albertini, A. M., Ferrari, E., Sonenshein, A. L., and Belitsky, B. R. 2016. “Interplay of CodY and ScoC in the regulation of major extracellular protease genes of Bacillus subtilis”, Journal of Bacteriology, 198(6), 907-920.
Becher, D., Büttner, K., Moche, M., Heßling, B., Hecker, M. 2011. “From the genome sequence to the protein inventory of Bacillus subtilis”, Proteomics, 11(15), 2971-2980.
Belitsky, B. R. and Sonenshein, A. L. 2013. “Genome-wide identification of Bacillus subtilis CodY-binding sites at single- nucleotide resolution”, Proceedings of the National Academy of Sciences, 110(17), 7026-7031.
Bernhardt, J., Weibezahn, J., Scharf, C., Hecker, M., 2003. “Bacillus subtilis during feast and famine: Visualization of the overall regulation of protein synthesis during glucose starvation by proteome analysis”, Genome Research, 13, 224-237.
Blencke HM, Homuth G, Ludwig H, Mäder U, Hecker M, Stülke J. Transcriptional profiling of gene expression in response to glucose in Bacillus subtilis: regulation of the central metabolic pathways. Metabolic Engineering. 2003. 5(2):133-49.
Brown, K. J., Formolo, C., Seol, H., Marathi, R. L., An, E., Pillai, D., Rood, B. R. 2012. “Advances in the proteomic investigation of the cell secretome”. Expert Review Proteomics, 9(3), 337-345.
Budde, I., Steil, L., Scharf, C., Völker U., Bremer, E. 2006. “Adaptation of Bacillus subtilis to growth at low temperature: a combined transcriptomic and proteomic appraisal. Microbiology”, 152(3), 831-853.
Bustin, S. A., Benes, V., Nolan, T., & Pfaffl, M. W. (2005). Quantitative real-time RT-PCR–a perspective. Journal of molecular endocrinology, 34(3), 597-601.
Büttner, K., Bernhardt, J., Scharf, C., Schmid, R., Mäder, U., Eymann, C., Hecker, M. 2001. “A comprehensive two-dimensional map of cytosolic proteins of Bacillus subtilis”, Electrophoresis, 22(14), 2908-2935.
Candela, T. and Fouet, A. 2006. “Poly‐gamma‐glutamate in bacteria”. Molecular Microbiology, 60(5), 1091-1098.
Cao, M., Kobel, P. A., Morshedi, M. M., Wu, M. F. W., Paddon, C., and Helmann, J. D. 2002. “Defining the Bacillus subtilis σ W regulon: A comparative analysis of promoter consensus search, run-off transcription/macroarray analysis (ROMA), and transcriptional profiling approaches”, Journal of Molecular Biology, 316(3), 443-457.
Casillas-Martinez, L., and P. Setlow. 1997. “Alkyl hydroperoxide reductase, catalase, MrgA, and superoxide dismutase are not involved in resistance of Bacillus subtilis spores to heat or oxidizing agents”, Journal of Bacteriology, 179, 7420-7425.
Chambert R, Pereira Y, Petit-Glatron MF (2003) Purification and characterization of YfkN, a trifunctional nucleotide phosphoesterase secreted by Bacillus subtilis. J Biochem 134:655-660.
Chen, L., James, L. P., and Helmann, J. D. 1993. “Metalloregulation in Bacillus subtilis: Isolation and characterization of two genes differentially repressed by metal ions”, Journal of Bacteriology, 175(17), 5428-5437.
Chi, B. K., Roberts, A. A., Huyen, T. T. T., Bäsell, K., Becher, D., Albrecht, D., ... and Antelmann, H. 2013. “S-bacillithiolation protects conserved and essential proteins against hypochlorite stress in firmicutes bacteria”, Antioxidants and Redox Signaling, 18(11), 1273-1295.
Chiancone, E., Ceci, P., Ilari, A., Ribacchi, F., and Stefanini, S. 2004. “Iron and proteins for iron storage and detoxification”. Biometals, 17(3), 197-202.
Chumsakul, O., Anantsri, D. P., Quirke, T., Oshima, T., Nakamura, K., Ishikawa, S., and Nakano, M. M. 2017. “Genome-Wide Analysis of ResD, NsrR, and Fur binding in Bacillus subtilis during anaerobic fermentative growth by in vivo footprinting”, Journal of Bacteriology, 199(13), e00086-17.
Chumsakul, O., Takahashi, H., Oshima, T., Hishimoto, T., Kanaya, S., Ogasawara, N., and Ishikawa, S. 2010. “Genome-wide binding profiles of the Bacillus subtilis transition state regulator AbrB and its homolog Abh reveals their interactive role in transcriptional regulation”, Nucleic Acids Research, 39(2), 414-428.
Dartois V, Débarbouillé M, Kunst F, Rapoport G. Characterization of a novel member of the DegS-DegU regulon affected by salt stress in Bacillus subtilis. Journal of Bacteriology. 1998. 180(7):1855-61
Débarbouillé M, Martin-Verstraete I, Arnaud M, Klier A, Rapoport G. Positive and negative regulation controlling expression of the sac genes in Bacillus subtilis.Research in Microbiology.1991. 142(7-8):757-64
Degering, C., Eggert, T., Puls, M., Bongaerts, J., Evers, S., Maurer, K. H., and Jaeger, K. E. 2010. “Optimization of protease secretion in Bacillus subtilis and Bacillus licheniformis by screening of homologous and heterologous signal peptides”, Applied and Environmental Microbiology, 76(19), 6370-6376.
Demir, M. 2013. “Proteome-Wıde Analysıs Of The Role Of Expressıon Of Bacılysın Operon On Idıophase Physıology Of B. subtilis” Yüksek Lisans Tez, ODTÜ, ANKARA.
Domínguez‐Cuevas, P., Porcelli, I., Daniel, R. A., and Errington, J. 2013. “Differentiated roles for MreB‐actin isologues and autolytic enzymes in Bacillus subtilis morphogenesis”, Molecular Microbiology, 89(6), 1084-1098.
Dragoš, A., Kovács, Á.T., Claessen, D. 2017. “The role of functional amyloids in multicellular growth and development of gram- positive bacteria”, Biomolecules,7(3), 60.
Ebner, P., Prax, M., Nega, M., Koch, I., Dube, L., Yu, W., ... ,Götz, F. 2015. “Excretion of cytoplasmic proteins (ECP) in Staphylococcus aureus”. Molecular Microbiology, 97(4), 775-789.
Eichenberger, P., Fujita, M., Jensen, S. T., Conlon, E. M., Rudner, D. Z., Wang, S. T., ... and Losick, R. 2004. “The program of gene transcription for a single differentiating cell type during sporulation in Bacillus subtilis”, PLoS Biology, 2(10), e328.
Ellermeier, C. D., Hobbs, E. C., Gonzalez-Pastor, J. E., and Losick, R. 2006. “A three-protein signaling pathway governing immunity to a bacterial cannibalism toxin”, Cell, 124(3), 549-559.
Eymann, C., Dreisbach, A., Albrecht, D., Bernhardt, J., Becher, D., Gentner, S., Tam, L. T., Büttner, K., Buurman, G., Scharf, C., Venz, S., Völker, U., Hecker, M. 2004. “A comprehensive proteome map of growing Bacillus subtilis cells”. Proteomics, 4(10), 2849-2876.
Fasehee H, Westers H, Bolhuis A, Antelmann H, Hecker M, Quax WJ, Mirlohi AF, van Dijl JM, Ahmadian, G. (2011) Functional analysis of the sortase YhcS in Bacillus subtilis. Proteomics, 11:3905-3913.
Fleige, S., & Pfaffl, M. W. (2006). RNA integrity and the effect on the real-time qRT-PCR performance. Molecular aspects of medicine, 27(2-3), 126-139.
Fouet, A., Sonenshein, A. L. 1990. “A target for carbon source-dependent negative regulation of the citB promoter of Bacillus subtilis”, Journal of Bacteriology, 172(2), 835-844.
Gao, H., Jiang, X., Pogliano, K., and Aronson, A. I. 2002. “The E1β and E2 subunits of the Bacillus subtilis pyruvate dehydrogenase complex are involved in regulation of sporulation”, Journal of Bacteriology, 184(10), 2780-2788.
Garti-levi, S., Eswara, A., Smith, Y., Fujita, M., Ben-Yehuda, S. 2013. “Novel modulators controlling entry into sporulation in Bacillus subtilis”, Journal of Bacteriology, 195(7), 1475-1483.
Gerth, U., Kock, H., Kusters, I., Michalik, S., Switzer, R. L., and Hecker, M. 2008. “Clp-dependent proteolysis down-regulates central metabolic pathways in glucose-starved Bacillus subtilis”, Journal of Bacteriology, 190(1), 321-331.
Gilois, N., Ramarao, N., Bouillaut, L., Perchat, S., Aymerich, S., Nielsen-LeRoux, C.,Gohar, M. 2007. “Growth-related variations in the Bacillus cereus secretome”, Proteomics, 7(10), 1719-1728.
Görg, A., Weiss, W., and Dunn, M. J. 2004. “Current two-dimensional electrophoresis technology for proteomics”, Proteomics, 4(12), 3665-3685.
Greenbaum, D., Luscombe, N. M., Jansen, R., Qian, J., Gerstein, M. 2001. “Interrelating different types of genomic data, from proteome to secretome:’oming in on function”, Genome Research, 11(9), 1463.
Griebel, A., Obermaier, C., Westermeier, R., Moche, M., Büttner, K. (2013). Simplification and Improvement of protein detection in two-dimensional electrophoresis gels with SERVA HPETM Lightning Red. Archives of physiology and biochemistry, 119(3), 94- 99.
Gyan, S., Shiohira, Y., Sato, I., Takeuchi, M., and Sato, T. 2006. “Regulatory loop between redox sensing of the NADH/NAD+ ratio by Rex (YdiH) and oxidation of NADH by NADH dehydrogenase Ndh in Bacillus subtilis”, Journal of Bacteriology, 188(20), 7062-7071.
Hamon, M. A., Stanley, N. R., Britton, R. A., Grossman, A. D., and Lazazzera, B. A. 2004. “Identification of AbrB‐regulated genes involved in biofilm formation by Bacillus subtilis”. Molecular Microbiology, 52(3), 847-860.
Hecker, M., Reder, A., Fuchs, S., Pagels, M., and Engelmann, S. (2009) Physiological proteomics and stress/starvation responses in Bacillus subtilis and Staphylococcus aureus. Res Microbiol 160(4):245-258.
Hirose, I., Sano, K., Shioda, I., Kumano, M., Nakamura, K. Yamane, K. 2000. “Proteome analysis of Bacillus subtilis extracellular proteins: a two-dimensional protein electrophoretic study”, Microbiology, 146, 65-75.
Hoch, J. A. (2017). A life in Bacillus subtilis signal transduction. Annual review of microbiology, 71, 1-19.
Höper, D., Bernhardt, J. Hecker, M. 2006. “Salt stress adaptation of Bacillus subtilis: A physiological proteomics approach”, Proteomics, 6, 1550-1562.
Hosoya, S., Lu, Z., Ozaki, Y., Takeuchi, M., and Sato, T. 2007. “Cytological analysis of the mother cell death process during sporulation in Bacillus subtilis”, Journal of Bacteriology, 189(6), 2561-2565.
Inaoka, T., Takahashi, K., Ohnishi-Kameyama, M., Yoshida, M., Ochi, K. 2003. “Guanine nucleotides guanosine 5’-diphosphate 3’-diphosphate and GTP cooperatively regulate the production of an antibiotic bacilysin in Bacillus subtilis”. Journal of Biology and Chemistry. 278, 2169-2176.
Inaoka, T., Wang, G., & Ochi, K. (2009). ScoC regulates bacilysin production at the transcription level in Bacillus subtilis. Journal of bacteriology, 191(23), 7367-7371.
Jahn, C. E., Charkowski, A. O., & Willis, D. K. (2008). Evaluation of isolation methods and RNA integrity for bacterial RNA quantitation. Journal of microbiological methods, 75(2), 318-324.
Jamroskovic, J., Chromikova, Z., List, C., Bartova, B., Barak, I., and Bernier-Latmani, R. (2016). Variability in DPA and Calcium Content in the Spores of Clostridium Species. Frontiers in microbiology, 7.
Jarmer, H., Berka, R., Knudsen, S., and Saxild, H. H. 2002. “Transcriptome analysis documents induced competence of Bacillus subtilis during nitrogen limiting conditions”, FEMS Microbiology Letters, 206(2), 197-200.
Jongbloed, J. D., Grieger, U., Antelmann, H., Hecker, M., Nijland, R., Bron, S., and Van Dijl, J. M. 2004. “Two minimal Tat translocases in Bacillus”. Molecular Microbiology, 54(5), 1319-1325.
Kaan, T., Homuth, G., Mäder, U., Bandow, J., and Schweder, T. 2002. “Genome-wide transcriptional profiling of the Bacillus subtilis cold-shock response”, Microbiology, 148(11), 3441-3455.
Kaffarnik, F. A., Jones, A. M., Rathjen, J. P., and Peck, S. C. 2009. “Effector proteins of the bacterial pathogen Pseudomonas syringae alter the extracellular proteome of the host plant, Arabidopsis thaliana”, Molecular and Cellular Proteomics, 8(1), 145- 156.
Kanamaru, K., Stephenson, S., and Perego, M. 2002. “Overexpression of the PepF oligopeptidase inhibits sporulation initiation in Bacillus subtilis”, Journal of Bacteriology, 184(1), 43-50.
Kang, M. S., Kim, S. R., Kwack, P., Lim, B. K., Ahn, S. W., Rho, Y. M., ... and Chung, C. H. (2003). Molecular architecture of the ATP‐dependent CodWX protease having an N‐terminal serine active site. The EMBO journal, 22(12), 2893-2902.
Karatas, A.Y., Cetin, S. and Ozcengiz, G. (2003). The effects of insertional mutations in comQ, comP, srfA, spo0H, spo0A and abrB genes on bacilysin biosynthesis in Bacillus subtilis. Biochimica et Biophysica Acta (BBA)-Gene Structure and Expression 1626(1), 51-56.
Kenig, M. ve Abraham, E.P. 1976. “Antimicrobial activities and antagonists of bacilysin and anticapsin”, Journal of General Microbiolology, 94, 37-45.
Kerff, F., Amoroso, A., Herman, R., Sauvage, E., Petrella, S., Filée, P., ... and Cosgrove, D. J. 2008. “Crystal structure and activity of Bacillus subtilis YoaJ (EXLX1), a bacterial expansin that promotes root colonization”. Proceedings of the National Academy of Sciences, 105(44), 16876-16881.
Kho CW, Park SG, Cho S, Lee DH, Myung PK, Park BC (2005) Confirmation of Vpr as a fibrinolytic enzyme present in extracellular proteins of Bacillus subtilis. Protein Expr Purif 39:1-7.
Kim, D., Yu, B. J., Kim, J., Lee, Y. J., Choi, S. G., Kang, S., and Pan, J. G. (2013). “The acetylproteome of gram‐positive model bacterium Bacillus subtilis”, Proteomics, 13(10-11), 1726-1736.
Kim, Y., Edwards, N., and Fenselau, C. 2016. “Extracellular vesicle proteomes reflect developmental phases of Bacillus subtilis”, Clinical Proteomics, 13(1), 6. Klein, D. (2002). Quantification using real-time PCR technology: applications and limitations. Trends in molecular medicine, 8(6), 257-260.
Kobayashi, K. (2007). Gradual activation of the response regulator DegU controls serial expression of genes for flagellum formation and biofilm formation in Bacillus subtilis. Molecular microbiology, 66(2), 395-409.
Kontinen, V. P., Sarvas, M. 1993. “The PrsA lipoprotein is essential for protein secretion in Bacillus subtilis and sets a limit for high‐level secretion”. Molecular Microbiology, 8(4), 727-737.
Köroğlu, T., Öğülür, I., Mutlu, S., Yazgan-Karataş, A., Ozcengiz, G. 2011. “Global regulatory systems operating in bacilysin biosynthesis in Bacillus subtilis”. Journal of Molecular Microbiology and Biotechnology, 20(3), 144-155.
Kouwen TR, van der Ploeg R, Antelmann H, Hecker M, Homuth G, Mäder U, van Dijl JM (2009) Overflow of a hyper-produced secretory protein from the Bacillus Sec pathway into the Tat pathway for protein secretion as revealed by proteogenomics. Proteomics 9:1018-1032.
Krishnappa, L., Dreisbach, A., Otto, A., Goosens, V. J., Cranenburgh, R. M., Harwood, C. R., ..., van Dijl, J. M. 2013. “Extracytoplasmic proteases determining the cleavage and release of secreted proteins, lipoproteins, and membrane proteins in Bacillus subtilis”. Journal of Proteome Research, 12(9), 4101-4110.
Krishnappa, L., Monteferrante, C. G., Neef, J., Dreisbach, A., and van Dijl, J. M. 2014. “Degradation of extracytoplasmic catalysts for protein folding in Bacillus subtilis”, Applied and Environmental Microbiology, 80(4), 1463-1468.
Kulak, N. A., Pichler, G., Paron, I., Nagaraj, N., and Mann, M. 2014. “Minimal, encapsulated proteomic-sample processing applied to copy-number estimation in eukaryotic cells”, Nature Methods, 11(3), 319-324.
Kunst, F., Ogasawara, N, Moszer, I., Albertini, A.M., Alloni, G., Azevedo, V. 1997. “The complete genome sequence of the Gram-positive bacterium Bacillus subtilis”, Nature, 390, 249-256.
Lai, E. M., Phadke, N. D., Kachman, M. T., Giorno, R., Vazquez, S., Vazquez, J. A., ... and Driks, A. 2003. “Proteomic analysis of the spore coats of Bacillus subtilis and Bacillus anthracis”, Journal of Bacteriology, 185(4), 1443-1454.
Lamsa, A., Liu, W. T., Dorrestein, P. C., and Pogliano, K. 2012. “The Bacillus subtilis cannibalism toxin SDP collapses the proton motive force and induces autolysis”. Molecular Microbiology, 84(3), 486–500.
Larralde, R., Robertson, M. P., & Miller, S. L. (1995). Rates of decomposition of ribose and other sugars: implications for chemical evolution. Proceedings of the National Academy of Sciences, 92(18), 8158-8160.
Lee, E. Y., Choi, D. Y., Kim, D. K., Kim, J. W., Park, J. O., Kim, S., ... , Gho, Y. S. 2009. “Gram‐positive bacteria produce membrane vesicles: proteomics‐based characterization of Staphylococcus aureus derived membrane vesicles”, Proteomics, 9(24), 5425-5436.
Lesuisse E, Schanck K, Colson, C (1993) Purification and preliminary characterization of the extracellular lipase of Bacillus subtilis 168, an extremely basic pH‐tolerant enzyme. Eur J Biochem 216: 155-160.
Litzinger, S., Duckworth, A., Nitzsche, K., Risinger, C., Wittmann, V., and Mayer, C. 2010. ”Muropeptide rescue in Bacillus subtilis involves sequential hydrolysis by β-N-acetylglucosaminidase and N-acetylmuramyl-L-alanine amidase”, Journal of Bacteriology, 192(12), 3132-3143.
Luo, Y., and Helmann, J. D. 2012. “Analysis of the role of Bacillus subtilis σM in β‐lactam resistance reveals an essential role for c‐di‐AMP in peptidoglycan homeostasis”, Molecular Microbiology, 83(3), 623-639.
Mahlstedt SA, Fielding EN, Moore BS, Walsh CT. Prephenate decarboxylases: a new prephenate-utilizing enzyme family that performs nonaromatizing decarboxylation en route to diverse secondary metabolites. Biochemistry 2010; 49:9021–3.
Mahlstedt SA, Walsh CT. Investigation of anticapsin biosynthesis reveals a four-enzyme pathway to tetrahydrotyrosine in Bacillus subtilis. Biochemistry 2010;49:912–23.
Mäkelä, M. R., Hildén, K., and Lundell, T. K. 2010. “Oxalate decarboxylase: biotechnological update and prevalence of the enzyme in filamentous fungi”, Applied Microbiology and Biotechnology, 87(3), 801-814.
Mäntsälä P, Zalkin H (1980) Extracellular and membrane-bound proteases from Bacillus subtilis. J Bacteriol. 141:493-501.
Mariappan, A., Makarewicz, O., Chen, X. H., Borriss, R. 2012. “Two-component response regulator DegU controls the expression of bacilysin in plant-growth-promoting bacterium Bacillus amyloliquefaciens FZB42”, Journal of Molecular Microbiology and Biotechnology, 22(2), 114-125.
Martin I, Débarbouillé M, Ferrari E, Klier A, Rapoport G (1987) Characterization of the levanase gene of Bacillus subtilis which shows homology to yeast invertase. Mol Gen Genet 208:177-184.
Martin-Verstraete I, Stülke J, Klier A, Rapoport G (1995) Two different mechanisms mediate catabolite repression of the Bacillus subtilis levanase operon. J Bacteriol 177:6919-692.
Marvasi, M., Visscher, P. T., and Casillas Martinez, L. 2010. “Exopolymeric substances (EPS) from Bacillus subtilis: polymers and genes encoding their synthesis”, FEMS Microbiology Letters, 313(1), 1-9.
Mashburn‐Warren, L. M., & Whiteley, M. 2006. “Special delivery: vesicle trafficking in prokaryotes”, Molecular Microbiology, 61(4), 839-846.
Miethke, M., Monteferrante, C. G., Marahiel, M. A., and van Dijl, J. M. 2013. “The Bacillus subtilis EfeUOB transporter is essential for high-affinity acquisition of ferrous and ferric iron”, Biochimica et Biophysica Acta (BBA)-Molecular Cell Research, 1833(10), 2267-2278.
Mirel, D. B., Estacio, W. F., Mathieu, M., Olmsted, E., Ramirez, J. and Marquez-Magana, L. M. 2000. “Environmental regulation of Bacillus subtilis sigma(D)-dependent gene expression”, Journal of bacteriology, 182(11), 3055-3062
Molle, V., Nakaura, Y., Shivers, R.P., Yamaguchi, H., Losick, R., Fujita, Y. and Sonenshein, A.L. 2003. “Additional targets of the Bacillus subtilis global regulator CodY identified by chromatin immunoprecipitation and genome-wide transcript analysis”, Journal of Bacteriology, 185(6), 1911-1922.
Möller, M. C. andHederstedt, L. 2008. “Extracytoplasmic processes impaired by inactivation of trxA (thioredoxin gene) in Bacillus subtilis”, Journal of Bacteriology, 190(13), 4660-4665.
Mostertz, J., Scharf, C., Hecker, M. Homuth, G. 2004. “Transcriptome and proteome analysis of Bacillus subtilis gene expression in response to superoxide and peroxide stress”, Microbiology, 150, 497-512.
Nagler, K., Krawczyk, A. O., De Jong, A., Madela, K., Hoffmann, T., Laue, M., ... and Moeller, R. (2016). Identification of differentially expressed genes during Bacillus subtilis spore outgrowth in high-salinity environments using RNA sequencing. Frontiers in microbiology, 7
Nakano, M. M. and Zuber, P. 1990. “Molecular biology of antibiotic production in Bacillus”. Critical Reviews in Biotechnology. 10(3), 223-240.
Nel, A. J., Garnett, S., Blackburn, J. M., and Soares, N. C. (2015). Comparative reevaluation of FASP and enhanced FASP methods by LC–MS/MS. Journal of proteome research, 14(3), 1637-1642.
Neuhoff, V., Arold, N., Taube D, Ehrhardt W. 1988. “Improved staining of proteins in polyacrylamide gels including isoelectric focusing gels with clear background at nanogram sensitivity using Coomassie Brilliant Blue G-250 and R-250”, Electrophoresis 9, 255-62.
Newton GGF. Antibiotics from a strain of B. subtilis: bacilipin A and bacilipin-B and bacilysin. Br J Exp Pathol 1949;30:306–19.
Nguyen, H. B. T. and Schumann, W. 2012. “The sporulation control gene spo0M of Bacillus subtilis is a target of the FtsH metalloprotease”, Research in Microbiology, 163(2), 114-118.
Nicolas, P., Mäder, U., Dervyn, E., Rochat, T., Leduc, A., Pigeonneau, N., ... and Becher, D. 2012. “Condition-dependent transcriptome reveals high-level regulatory architecture in Bacillus subtilis”, Science, 335(6072), 1103-1106.
O'Farrell, P. H. (1975). High resolution two-dimensional electrophoresis of proteins. Journal of biological chemistry, 250(10), 4007-4021.
Orsburn, B. C., Melville, S. B., and Popham, D. L. 2010. “EtfA catalyses the formation of dipicolinic acid in Clostridium perfringens”, Molecular Microbiology, 75(1), 178-186.
Oussenko IA, Sanchez R, Bechhofer DH (2004) Bacillus subtilis YhcR, a high-molecular-weight, nonspecific endonuclease with a unique domain structure. J Bacteriol 186:5376-5383.
Özcengiz, G. ve Alaeddinoglu, N. G. 1991. “Bacilysin production by Bacillus subtilis: effects of bacilysin, pH and temperature”, Folia Microbiologica, 36, 522-526.
Özcengiz, G., Alaeddinoglu, N. G., Demain, A. L. 1990. “Regulation of biosynthesis of bacilysin by Bacillus subtilis”, Journal of Industrial Microbiology, 6, 91-100.
Özcengiz, G., ve Öğülür, İ. 2015. “Biochemistry, genetics and regulation of bacilysin biosynthesis and its significance more than an antibiotic”, New Biotechnology, 32(6), 612-619.
Parker JB, Walsh CT. Action and timing of BacC and BacD in the late stages of biosynthesis of the dipeptide antibiotic bacilysin. Biochemistry (NY) 2013; 52:889–901.
Parker JB, Walsh CT. Olefin isomerization regiochemistries during tandem action of BacA and BacB on prephenate in bacilysin biosynthesis. Biochemistry 2012;51:3241–51.
Parker JB, Walsh CT. Stereochemical outcome at four stereogenic centers during conversion of prephenate to tetrahydrotyrosine by BacABGF in the bacilysin pathway. Biochemistry 2012;51:5622–32.
Pereira, Y., Petit-Glatron, M. F., and Chambert, R. 2001. “yveB, encoding endolevanase LevB, is part of the sacB–yveB–yveA levansucrase tricistronic operon in Bacillus subtilis”, Microbiology, 147(12), 3413-3419.
Perry, D. ve Abraham, E. P. 1979. “Transport and metabolism of bacilysin and other peptides by suspensions of Staphylococcus aureus”, Journal of General Microbiology, 115, 213-221
Petersohn, A., Brigulla, M., Haas, S., Hoheisel, J. D., Völker, U., and Hecker, M. 2001. “Global analysis of the general stress response of Bacillus subtilis”, Journal of Bacteriology, 183(19), 5617-5631.
Pfaffl, M. W. (2001). A new mathematical model for relative quantification in real-time RT–PCR. Nucleic acids research, 29(9), e45-e45.
Pfaffl, M. W. (2012). Quantification strategies in real-time polymerase chain reaction. Quantitative real-time PCR. Appl Microbiol, 53-62.
Pfaffl, M. W., Tichopad, A., Prgomet, C., & Neuvians, T. P. (2004). Determination of stable housekeeping genes, differentially regulated target genes and sample integrity: BestKeeper–Excel-based tool using pair-wise correlations. Biotechnology letters, 26(6), 509-515.
Provvedi, R., Chen, I., and Dubnau, D. 2001. “NucA is required for DNA cleavage during transformation of Bacillus subtilis”, Molecular Microbiology, 40(3), 634-644.
Que, Q. and Helmann, J. D. 2000. “Manganese homeostasis in Bacillus subtilis is regulated by MntR, a bifunctional regulator related to the diphtheria toxin repressor family of proteins”, Molecular Microbiology, 35(6), 1454-1468.
Rajavel M, Gopal B. Analysis of multiple crystal forms of Bacillus subtilis BacB suggests a role for a metal ion as a nucleant for crystallization. Acta Crystallogr D 2010;66:635–9.
Rajavel M, Mitra A, Gopal B. Role of Bacillus subtilis BacB in the synthesis of bacilysin. J Biol Chem 2009;284:31882–92.
Rajavel M, Perinbam K, Gopal B. Structural insights into the role of Bacillus subtilis YwfH (BacG) in tetrahydrotyrosine synthesis. Acta Crystallogr D 2013;69:324–32.
Ramagli, L. S. ve Rodrigez, L. V. 1985. “Quantitation of microgram amounts of protein in two-dimensional polyacrylamide gel electrophoresis sample buffer”, Electrophoresis, 6, 559-563.
Rao DECS, Rao KV, Reddy VD (2008) Cloning and expression of Bacillus phytase gene (phy) in Escherichia coli and recovery of active enzyme from the inclusion bodies. J Appl Microbiol 105:1128-1137
Rao, X., Huang, X., Zhou, Z., & Lin, X. (2013). An improvement of the 2ˆ (–delta delta CT) method for quantitative real-time polymerase chain reaction data analysis. Biostatistics, bioinformatics and biomathematics, 3(3), 71.
Reder, A., Höper, D., Gerth, U., and Hecker, M. 2012. “The contribution of individual σB-dependent general stress genes to oxidative stress resistance of Bacillus subtilis”. Journal of Bacteriology, JB-00528.
Reents, H., Münch, R., Dammeyer, T., Jahn, D., and Härtig, E. 2006. “The Fnr regulon of Bacillus subtilis”, Journal of Bacteriology, 188(3), 1103-1112.
Reizer, J., Bachem, S., Reizer, A., Arnaud, M., Saier Jr, M. H., and Stülke, J. 1999. “Novel phosphotransferase system genes revealed by genome analysis–the complete complement of PTS proteins encoded within the genome of Bacillus subtilis”, Microbiology, 145(12), 3419-3429.
Richardson, D. J., Berks, B. C., Russell, D. A., Spiro, S., and Taylor, C. J. 2001. “Functional, biochemical and genetic diversity of prokaryotic nitrate reductases”, Cellular and Molecular Life Sciences CMLS, 58(2), 165-178.
Rivas LA, Parro V, Moreno-Paz M, Mellado RP (2000) The Bacillus subtilis 168 csn gene encodes a chitosanase with similar properties to a Streptomyces enzyme. Microbiol 146:2929-2936
Rogers HJ, Lomakina N, Abraham EP. Observations on the structure of bacilysin. Biochem J 1965;97:579–86.
Ruijter, J. M., Ramakers, C., Hoogaars, W. M. H., Karlen, Y., Bakker, O., Van den Hoff, M. J. B., & Moorman, A. F. M. (2009). Amplification efficiency: linking baseline and bias in the analysis of quantitative PCR data. Nucleic acids research, 37(6), e45- e45.
Sakajoh, M., Solomon, N. A., Demain, A. L. 1987. “Cell-free synthesis of the dipeptide antibiotic bacilysin”, Journal of Industrial Microbiology, 2, 201-208.
Salzberg LI, Botella E, Hokamp K, Antelmann H, Maaß S, Becher D, Noone D, Devine KM. Genome-wide analysis of phosphorylated PhoP binding to chromosomal DNA reveals several novel features of the PhoPR-mediated phosphate limitation response in Bacillus subtilis. Journal of Bacteriology. 2015. 197(8):1492-506.
Sansinenea, E., and Ortiz, A. (2011). Secondary metabolites of soil Bacillus spp. Biotechnology letters, 33(8), 1523-1538.
Scharf, C., Riethdorf, S., Ernst, H., Engelmann, S., Völker, U., and Hecker, M. 1998. “Thioredoxin is an essential protein induced by multiple stresses in Bacillus subtilis”, Journal of Bacteriology, 180(7), 1869-1877.
Schirner, K. and Errington, J. 2009. “The cell wall regulator σI specifically suppresses the lethal phenotype of mbl mutants in Bacillus subtilis”, Journal of Bacteriology, 191(5), 1404-1413.
Schroeder, J. W., & Simmons, L. A. (2013). Complete genome sequence of Bacillus subtilis strain PY79. Genome announcements, 1(6), e01085-13.
Serizawa M, Kodama K, Yamamoto H, Kobayashi K, Ogasawara N, Sekiguchi J. Functional analysis of the YvrGHb two- component system of Bacillus subtilis: identification of the regulated genes by DNA microarray and northern blot analyses.Bioscience, Biotechnology and Biochemistry. 2005. 69(11):2155-69.
Seydlová, G., Halada, P., Fišer, R., Toman, O., Ulrych, A., and Svobodová, J. 2012. “DnaK and GroEL chaperones are recruited to the Bacillus subtilis membrane after short‐term ethanol stress”, Journal of Applied Microbiology, 112(4), 765-774.
Simms, D., Cizdziel, P. E., & Chomczynski, P. (1993). TRIzol: A new reagent for optimal single-step isolation of RNA. Focus, 15(4), 532-535.
Smith JL, Grossman, AD (2015) In vitro whole genome DNA binding analysis of the bacterial replication initiator and transcription factor DnaA. PLoS Genet. 11: e1005258.
Solomon, J. M. ve Grossman, A. D. 1996. “Who’s competent and when: regulation of natural genetic competence in bacteria”, Trends in Genetics, 12, 150-155.
Stein, T. 2005. “Bacillus subtilis antibiotics: structures, syntheses, and specific functions”, Molecular Microbiology, 56(4), 845- 857.
Steinborn, G., Hajirezaei, M. R., Hofemeister, J. 2005. “bac genes for recombinant bacilysin and anticapsin production in Bacillus host strains”, Archieves of Microbiology, 183, 71-79.
Strauch, M. A., Bobay, B. G., Cavanagh, J., Yao, F., Wilson, A., and Le Breton, Y. 2007. “Abh and AbrB control of Bacillus subtilis antimicrobial gene expression”. Journal of Bacteriology, 189(21), 7720-7732.
Tam, L. T., Antelmann, H., Eymann, C., Albrecht, D. Bernhardt, J., Hecker, M. 2006. “Proteome signatures for stress and starvation in Bacillus subtilis as revealed by a 2-D gel image color coding approach”, Proteomics, 6, 4565-4585.
Tanovic, A., Samel, S. A., Essen, L. O., and Marahiel, M. A. 2008. “Crystal structure of the termination module of a nonribosomal peptide synthetase”, Science, 3215889, 659-663.
Taşkın, A. 2010. “Proteome-wide analysis of the functional roles of bacilysin biosynthesis in Bacillus subtilis”, Yüksek Lisans Tez, ODTÜ, ANKARA.
Tjalsma, H., Antelmann, H., Jongbloed, J. D., Braun, P. G. 2004. “Proteomics of protein secretion by Bacillus subtilis: Separating the “secrets” of the secretome”, Microbiology and Molecular Biology Reviews. 68, 207-33.
Töwe, S., Leelakriangsak, M., Kobayashi, K., Duy, N.V., Hecker, M., Zuber, P., and Antelmann, H. 2007. “TheMarR-type repressor MhqR (YkvE) regulates multiple dioxygenases/glyoxalases and an azoreductase which confer resistance to 2- methylhydroquinone and catechol in Bacillus subtilis”, Molecular Microbiology, 65: 40–54.
Tsukahara K, Ogura M (2008) Characterization of DegU-dependent expression of bpr in Bacillus subtilis. FEMS Microbiol Lett. 280:8-13.
Valasek, M. A., & Repa, J. J. (2005). The power of real-time PCR. Advances in physiology education, 29(3), 151-159.
Van Der Ploeg, R., Mäder, U., Homuth, G., Schaffer, M., Denham, E. L., Monteferrante, C. G., ... and Hecker, M. (2011). Environmental salinity determines the specificity and need for Tat-dependent secretion of the YwbN protein in Bacillus subtilis. PLoS One, 6(3), e18140.
van Dijl, J., & Hecker, M. (2013). Bacillus subtilis: from soil bacterium to super-secreting cell factory.
Van, Dijl, J. M., Braun, P. G., Robinson, C., Quax, W. J., Antelmann, H., Hecker, M., Jongbloed, J. D. H. 2002. “Functional genomic analysis of the Bacillus subtilis Tat pathway for protein secretion”, Journal of Biotechnology, 98(2-3), 243-254.
Vega-Cabrera, L. A., Guerrero, A., Rodríguez-Mejía, J. L., Tabche, M. L., Wood, C. D., Gutiérrez-Rios, R. M., ... and Pardo- López, L. 2017. “Analysis of Spo0M function in Bacillus subtilis”, PloS One, 12(2), e0172737.
Vitikainen, M., Lappalainen, I., Seppala, R., Antelmann, H., Boer, H., Taira, S., ... and Kontinen, V. P. 2004. “Structure-function analysis of PrsA reveals roles for the parvulin-like and flanking N-and C-terminal domains in protein folding and secretion in Bacillus subtilis”, Journal of Biological Chemistry, 279(18), 19302-1931
Voigt, B., Antelmann, H., Albrecht, D., Ehrenreich, A., Maurer, K. H., Evers, S., ... and Hecker, M. 2009. “Cell physiology and protein secretion of Bacillus licheniformis compared to Bacillus subtilis”, Journal of Molecular Microbiology and Biotechnology, 16(1-2), 53-68.
Voigt, B., Schweder, T., Sibbald, M. J. J. B., Albrecht, D., Ehrenreich, A., Bernhardt, J., Feesche J., Maurer K. H., Gottschalk, G., Van Djil J. M., Hecker, M. 2006. “The extracellular proteome of Bacillus licheniformis grown in different media and under different nutrient starvation conditions”, Proteomics, 6(1), 268-281.
Wahlström, E., Vitikainen, M., Kontinen, V. P., and Sarvas, M. 2003. “The extracytoplasmic folding factor PrsA is required for protein secretion only in the presence of the cell wall in Bacillus subtilis”, Microbiology, 149(3), 569-577.
Walker, J. E. ve Abraham, E. P. 1970. “The structure of bacilysin and other products of Bacillus subtilis”, Biochemistry Journal 118, 563-570.
Walton, R. B., Rickes, E. L.1962. “Reversal of the antibiotic, bacillin, by N-acetylglucosamine”, Journal of Bacteriology, 84, 1148- 1151.
Wenzel, M., Chiriac, A. I., Otto, A., Zweytick, D., May, C., Schumacher, C., ... and Erdmann, R. 2014. “Small cationic antimicrobial peptides delocalize peripheral membrane proteins”, Proceedings of the National Academy of Sciences, 111(14), 1409-1418.
Wenzel, M., Kohl, B., Münch, D., Raatschen, N., Albada, H. B., Hamoen, L., ... and Bandow, J. E. 2012. “Proteomic response of Bacillus subtilis to lantibiotics reflects differences in interaction with the cytoplasmic membrane”, Antimicrobial Agents and Chemotherapy, 56(11), 5749-5757.
Widner, B., Behr, R., Von Dollen, S., Tang, M., Heu, T., Sloma, A., Sternberg, D., DeAngelis, P. L., Weigel, P. H., Brown S. 2005. “Hyaluronic Acid Production in Bacillus subtilis”, Applied and Environmental Microbiology, 71(7), 3747-3752.
Winkler, W. C., Nahvi, A., Roth, A., Collins, J. A., and Breaker, R. R. (2004). Control of gene expression by a natural metabolite- responsive ribozyme. Nature, 428(6980), 281.
Wipat, A. ve Harwood, C. R. 1999. “The Bacillus subtilis genome sequence: The molecular blueprint of a soil bacterium”, FEMS Microbiology Ecology, 28(1), 1-9.
Wisniewski, J. R., Zougman, A., Nagaraj, N., Mann, M. 2009. “Universal sample preparation method for proteome analysis”, Nature methods, 6(5), 359.
Yamane, K., Bunai, K., Kakeshita, H. 2004. “Protein traffic for secretion and related machinery of Bacillus subtilis”, Bioscience, Biotechnology and Biochemistry, 68(10), 2007-2023.
Yang, C. K., Zhang, X. Z., Lu, C. D., Tai, P. C. 2014. “An internal hydrophobic helical domain of Bacillus subtilis enolase is essential but not sufficient as a non-cleavable signal for its secretion”, Biochemical and Biophysical Research Communications, 446(4), 901-905.
Yang, C.-K., Ewis, H. E., Zhang, X., Lu, C.-D., Hu, H.-J., Pan, Y.,Tai, P. C. 2011. “Nonclassical protein secretion by Bacillus subtilis in the stationary phase is not due to cell lysis”, Journal of Bacteriology, 193(20), 5607-15.
Yazgan, A., Özcengiz, G. Marahiel, M. H. 2001. “Tn 10 insertional mutations of Bacillus subtilis that block the biosynthesis of bacilysin”, Biochimica et Biophysica Acta 1518:87-94.
Ye, W. R., Tao, W., Bedzyk, L., Young, T., Chen, M., and Li, L. 2000. “Global gene expression profiles of Bacillus subtilis grown under anaerobic conditions”, Journal of Bacteriology, 182(16), 4458-4465.
Yoshida, K. I., Yamaguchi, H., Kinehara, M., Ohki, Y. H., Nakaura, Y., and Fujita, Y. 2003. “Identification of additional TnrA‐ regulated genes of Bacillus subtilis associated with a TnrA box”, Molecular Microbiology, 49(1), 157-165.
Zawadzka, A. M., Kim, Y., Maltseva, N., Nichiporuk, R., Fan, Y., Joachimiak, A., & Raymond, K. N. 2009. “Characterization of a Bacillus subtilis transporter for petrobactin, an anthrax stealth siderophore”, Proceedings of the National Academy of Sciences, 106(51), 21854-21859.

APA	ÖZCENGİZ G, İŞLEREL E (2018). Bacillus subtilis Standart Suş (PY79) ile Basilisinin Bloke Edildiği Suşun (OGU1) Karşılaştırmalı Dinamik Sekretom Analizi. , 1 - 80.
Chicago	ÖZCENGİZ Gülay,İŞLEREL Elif Tekin Bacillus subtilis Standart Suş (PY79) ile Basilisinin Bloke Edildiği Suşun (OGU1) Karşılaştırmalı Dinamik Sekretom Analizi. (2018): 1 - 80.
MLA	ÖZCENGİZ Gülay,İŞLEREL Elif Tekin Bacillus subtilis Standart Suş (PY79) ile Basilisinin Bloke Edildiği Suşun (OGU1) Karşılaştırmalı Dinamik Sekretom Analizi. , 2018, ss.1 - 80.
AMA	ÖZCENGİZ G,İŞLEREL E Bacillus subtilis Standart Suş (PY79) ile Basilisinin Bloke Edildiği Suşun (OGU1) Karşılaştırmalı Dinamik Sekretom Analizi. . 2018; 1 - 80.
Vancouver	ÖZCENGİZ G,İŞLEREL E Bacillus subtilis Standart Suş (PY79) ile Basilisinin Bloke Edildiği Suşun (OGU1) Karşılaştırmalı Dinamik Sekretom Analizi. . 2018; 1 - 80.
IEEE	ÖZCENGİZ G,İŞLEREL E "Bacillus subtilis Standart Suş (PY79) ile Basilisinin Bloke Edildiği Suşun (OGU1) Karşılaştırmalı Dinamik Sekretom Analizi." , ss.1 - 80, 2018.
ISNAD	ÖZCENGİZ, Gülay - İŞLEREL, Elif Tekin. "Bacillus subtilis Standart Suş (PY79) ile Basilisinin Bloke Edildiği Suşun (OGU1) Karşılaştırmalı Dinamik Sekretom Analizi". (2018), 1-80.

APA	ÖZCENGİZ G, İŞLEREL E (2018). Bacillus subtilis Standart Suş (PY79) ile Basilisinin Bloke Edildiği Suşun (OGU1) Karşılaştırmalı Dinamik Sekretom Analizi. , 1 - 80.
Chicago	ÖZCENGİZ Gülay,İŞLEREL Elif Tekin Bacillus subtilis Standart Suş (PY79) ile Basilisinin Bloke Edildiği Suşun (OGU1) Karşılaştırmalı Dinamik Sekretom Analizi. (2018): 1 - 80.
MLA	ÖZCENGİZ Gülay,İŞLEREL Elif Tekin Bacillus subtilis Standart Suş (PY79) ile Basilisinin Bloke Edildiği Suşun (OGU1) Karşılaştırmalı Dinamik Sekretom Analizi. , 2018, ss.1 - 80.
AMA	ÖZCENGİZ G,İŞLEREL E Bacillus subtilis Standart Suş (PY79) ile Basilisinin Bloke Edildiği Suşun (OGU1) Karşılaştırmalı Dinamik Sekretom Analizi. . 2018; 1 - 80.
Vancouver	ÖZCENGİZ G,İŞLEREL E Bacillus subtilis Standart Suş (PY79) ile Basilisinin Bloke Edildiği Suşun (OGU1) Karşılaştırmalı Dinamik Sekretom Analizi. . 2018; 1 - 80.
IEEE	ÖZCENGİZ G,İŞLEREL E "Bacillus subtilis Standart Suş (PY79) ile Basilisinin Bloke Edildiği Suşun (OGU1) Karşılaştırmalı Dinamik Sekretom Analizi." , ss.1 - 80, 2018.
ISNAD	ÖZCENGİZ, Gülay - İŞLEREL, Elif Tekin. "Bacillus subtilis Standart Suş (PY79) ile Basilisinin Bloke Edildiği Suşun (OGU1) Karşılaştırmalı Dinamik Sekretom Analizi". (2018), 1-80.