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Investigation of Antimicrobial Activities and 16S rRNA Sequences of Actinomycetes Isolated from Karst Caves in the Eastern Black Sea Region of Türkiye

Yıl 2023, Cilt: 26 Sayı: 6, 1277 - 1290, 31.12.2023

Enis Fuat Tüfekci , Ümit Uzun , Nagihan Sağlam Ertunga , Ayşenur Biber , İnanç Alptuğ Hıdıroğlu , İlayda Tekkılıç , Birhan Altay , Ali Osman Kılıç

https://doi.org/10.18016/ksutarimdoga.vi.1226184
Cited By: 1

Öz

Considering that most antibiotics originate from actinomycete group bacteria, especially the Streptomyces genus, it is predicted that novel actinomycetes isolated from extreme environments such as caves may bring novel antibiotics to the medical world. The study aimed to screen the antimicrobial activity of actinomycetes isolated from the three karst caves in Türkiye and to identify selected isolates with antimicrobial activity by molecular methods. One hundred seventy-nine actinomycetes isolated from Akçakale, Kırklar (Altıntaş), and Köprübaşı Caves in Gümüşhane province in the Eastern Black Sea Region of Türkiye were included in the study. The antimicrobial activity of isolates was investigated using the modified cross-streak agar method against seven Gram-negative bacteria, three Gram-positive bacteria, and one yeast strain. Fifty-three isolates (29.6%) had antimicrobial activity against at least one of the tested microorganisms. The rate of isolates exhibiting antimicrobial activity against Staphylococcus aureus, Bacillus subtilis, Enterococcus faecalis, Chromobacterium violaceum, Klebsiella pneumoniae, Salmonella Typhimurium, Escherichia coli, Acinetobacter haemolyticus, Pseudomonas aeruginosa, Enterobacter aerogenes, and Candida albicans was 21.2%, 20.0%, 16.8%, 12.8%, 3.4%, 2.8%, 2.2%, 1.1%, 0.6%, 0.6%, and 0.6%, respectively. An actinomycete isolate, TRMS 124, showed antimicrobial activity against ten test microorganisms. The 16S ribosomal RNA (16S rRNA) sequencing was performed for the identification and phylogenetic analysis of 26 isolates randomly selected among actinomycetes that exhibited antimicrobial activity against at least three test microorganisms. As a result, it was determined that 24 isolates showed homology with various Streptomyces species and two isolates with Embleya scabrispora and Couchioplanes caeruleus, respectively. These results showed that karst caves could be good sources for isolating actinomycetes with the potential to produce antimicrobial compounds.

Anahtar Kelimeler

16S ribosomal RNA Actinomycetes Antimicrobial activity Cave Streptomyces

Proje Numarası

FBA-2016-5481

Kaynakça

  • Alisjahbana, B., Debora, J., Susandi, E., & Darmawan, G. (2021). Chromobacterium violaceum: A review of an unexpected scourge. International Journal of General Medicine, 14, 3259-3270. https://doi.org/ 10.2147/IJGM.S272193
  • Bedel, H. (2020). Farklı Habitatlardan Toplanan Toprak ve Su Kaynaklarındaki Aktinomisetlerin İzolasyonu, Tanımlanmasi ve Antibakteriyel Aktivitenin Belirlenmesi (Tez No 663288). [Yüksek Lisans Tezi, Burdur Mehmet Akif Ersoy Üniversitesi Fen Bilimleri Enstitüsü Gıda Mühendisliği Ana Bilim Dalı]. Yükseköğretim Kurulu Ulusal Tez Merkezi.
  • Belyagoubi, L., Belyagoubi-Benhammou, N., Jurado, V., Dupont, J., Lacoste, S., Djebbah, F., Ounadjela, F.Z., Benaissa, S., Habi, S., Abdelouahi, D.E., & Saiz-Jimenez, C. (2018). Antimicrobial activities of culturable microorganisms (actinomycetes and fungi) isolated from Chaabe Cave, Algeria. International Journal of Speleology, 47(2), 189-199. https://doi.org/10.5038/1827-806X.47.2.2148
  • Cheeptham, N., Sadoway, T., Rule, D., Watson, K., Moote, P., Soliman, L.C., Azad, N., Donkor, K.K., & Horne, D. (2013). Cure from the cave: volcanic cave actinomycetes and their potential in drug discovery. International Journal of Speleology, 42(1), 35-47. http://dx.doi.org/10.5038/1827-806X.42.1.5
  • Chen, W.P. & Kuo, T.T. (1993). A simple and rapid method for the preparation of gram-negative bacterial genomic DNA. Nucleic acids research, 21(9), 2260. https://doi.org/10.1093/nar/21.9.2260
  • Devanshi, S., Shah, K.R., Arora, S. & Saxena, S. (2021). Actinomycetes as an environmental scrubber. In Abdel-Raouf, M.E., & El-Keshawy, M.H. (Eds.), Crude oil - new technologies and recent approaches. IntechOpen, London.
  • Doğruöz-Güngör, N., Çandıroğlu, B., & Altuğ, G. (2020). Enzyme profiles and antimicrobial activities of bacteria isolated from the Kadiini Cave, Alanya, Turkey. Journal of Cave and Karst Studies, 82(2), 106-115. https://doi.org/10.4311/2019MB0107
  • Farda, B., Djebaili, R., Vaccarelli, I., Del Gallo, M., & Pellegrini, M. (2022). Actinomycetes from caves: An overview of their diversity, biotechnological properties, and insights for their use in soil environments. Microorganisms, 10(2), 453. https:// doi.org/10.3390/microorganisms10020453
  • Farhana, A. & Khan, Y.S (2022). Biochemistry, Lipopolysaccharide. In: StatPearls [Internet]. Treasure Island (FL): StatPearls Publishing. Available from: https://www.ncbi.nlm.nih.gov/ books/NBK554414/ (Accessed on 1 May 2023).
  • Guo, Y., Zheng, W., Rong, X., & Huang, Y. (2008). A multilocus phylogeny of the Streptomyces griseus 16S rRNA gene clade: Use of multilocus sequence analysis for streptomycete systematics. International Journal of Systematic and Evolutionary Microbiology, 58(1), 149-159. https:// doi.org/10.1099/ijs.0.65224-0
  • Hamedi, J., Kafshnouchi, M., & Ranjbaran, M. (2019). A study on actinobacterial diversity of Hampoeil cave and screening of their biological activities. Saudi Journal of Biological Sciences, 26(7), 1587-1595. https://doi.org/10.1016/j.sjbs.2018.10.010
  • Herold, K., Gollmick, F.A., Groth, I., Roth, M., Menzel, K.D., Möllmann, U., Gräfe, U., & Hertweck, C. (2005). Cervimycin A-D: a polyketide glycoside complex from a cave bacterium can defeat vancomycin resistance. Chemistry (Weinheim an der Bergstrasse, Germany), 11(19), 5523-5530. https://doi.org/10.1002/chem.200500320
  • Hibbing, M.E., Fuqua, C., Parsek, M.R., & Peterson, S.B. (2010). Bacterial competition: surviving and thriving in the microbial jungle. Nature Reviews Microbiology, 8(1), 15-25. https://doi.org/10.1038/ nrmicro2259
  • Jaroszewicz, W., Bielańska, P., Lubomska, D., Kosznik-Kwaśnicka, K., Golec, P., Grabowski, Ł., Wieczerzak, E., Dróżdż, W., Gaffke, L., Pierzynowska, K., Węgrzyn, G., & Węgrzyn, A. (2021). Antibacterial, antifungal and anticancer activities of compounds produced by newly isolated Streptomyces strains from the Szczelina Chochołowska Cave (Tatra Mountains, Poland). Antibiotics (Basel, Switzerland), 10(10): 1212. https://doi.org/10.3390/antibiotics10101212
  • Kimura, M. (1980). A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution, 16(2), 111-120. https://doi.org/10.1007/BF01731581
  • Kováč, Ľ. (2018). Caves as oligotrophic ecosystems. In: Moldovan, O., Kováč, Ľ. & Halse, S. (Eds.), Cave ecology. Springer: Cham, Switzerland.
  • Labeda, D.P. (2011). Multilocus sequence analysis of phytopathogenic species of the genus Streptomyces. International Journal of Systematic and Evolutionary Microbiology, 61(10), 2525-2531. https://doi.org/10.1099/ijs.0.028514-0
  • Long, Y., Jiang, J., Hu, X., Zhou, J., Hu, J., & Zhou, S. (2019). Actinobacterial community in Shuanghe Cave using culture-dependent and -independent approaches. World Journal of Microbiology & Biotechnology, 35(10), 153. https://doi.org/ 10.1007/ s11274-019-2713-y
  • Maciejewska, M., Adam, D., Martinet, L., Naômé, A., Całusińska, M., Delfosse, P., Carnol, M., Barton, H. A., Hayette, M. P., Smargiasso, N., De Pauw, E., Hanikenne, M., Baurain, D., & Rigali, S. (2016). A phenotypic and genotypic analysis of the antimicrobial potential of cultivable Streptomyces isolated from cave moonmilk deposits. Frontiers in Microbiology, 7,1455. https://doi.org/10.3389/ fmicb.2016.01455
  • Miethke, M., Pieroni, M., Weber, T., Brönstrup, M., Hammann, P., Halby, L., Arimondo, P.B., Glaser, P., Aigle, B., Bode, H.B., Moreira, R., Li, Y., Luzhetskyy, A., Medema, M.H., Pernodet, J.L., Stadler, M., Tormo, J.R., Genilloud, O., Truman, A.W., … Müller, R. (2021). Towards the sustainable discovery and development of new antibiotics. Nature Reviews Chemistry, 5(10), 726-749. https://doi.org/10.1038/s41570-021-00313-1
  • Nimaichand, S., Devi, A.M., Tamreihao, K., Ningthoujam, D.S., & Li, W.J. (2015). Actinobacterial diversity in limestone deposit sites in Hundung, Manipur (India) and their antimicrobial activities. Frontiers in Microbiology, 6, 413. https://doi.org/10.3389/fmicb.2015.00413
  • Pradana, A.D., Sekarini, D.N., Suma, A.A., & Maliza, R. (2022). Study on the antibacterial effect from moonmilk Pindul Cave, Indonesia. Iranian Journal of Medical Microbiology, 16(2), 165-172. https://doi.org/10.30699/ijmm.16.2.165
  • Procópio, R.E., Silva, I.R., Martins, M.K., Azevedo, J.L., & Araújo, J.M. (2012). Antibiotics produced by Streptomyces. The Brazilian journal of infectious diseases: an official publication of the Brazilian Society of Infectious Diseases, 16(5), 466-471. https://dx.doi.org/10.1016/j.bjid.2012.08.014
  • Prudence, S.M.M., Addington, E., Castaño-Espriu, L., Mark, D.R., Pintor-Escobar, L., Russell, A.H., & McLean, T.C. (2020). Advances in actinomycete research: An ActinoBase review of 2019. Microbiology (Reading, England), 166(8), 683-694. https://dx.doi.org/10.1099/mic.0.000944
  • Rangseekaew, P. & Pathom-Aree, W. (2019). Cave actinobacteria as producers of bioactive metabolites. Frontiers in Microbiology, 10, 387. https://dx.doi.org/10.3389/fmicb.2019.00387
  • Rong, X. & Huang, Y. (2012). Taxonomic evaluation of the Streptomyces hygroscopicus clade using multilocus sequence analysis and DNA-DNA hybridization, validating the MLSA scheme for systematics of the whole genus. Systematic and Applied Microbiology, 35(1), 7-18. https://dx.doi.org/ 10.1016/j.syapm.2011.10.004
  • Saitou, N. & Nei, M. (1987). The neighbor-joining method: a new method for reconstructing phylogenetic trees. Molecular Biology and Evolution, 4(4), 406-425. https://dx.doi.org/10.1093/ oxfordjournals.molbev.a040454
  • Selim, M.S.M., Abdelhamid, S.A., & Mohamed, S.S. (2021). Secondary metabolites and biodiversity of actinomycetes. Journal, Genetic Engineering & Biotechnology, 19(1), 72. https://doi.org/10.1186/ s43141-021-00156-9
  • SPSS, (2015). IBM SPSS Statistics 23.0 for Windows. Armonk, NY.
  • Syiemiong, D. & Jha, D.K. (2019). Antibacterial potential of actinobacteria from a limestone mining site in Meghalaya, India. Journal of Pure and Applied Microbiology, 13(2), 789-802. https:// dx.doi.org/10.22207/JPAM.13.2.14
  • Tamura, K., Stecher, G., & Kumar, S. (2021). MEGA 11: Molecular evolutionary genetics analysis version 11. Molecular Biology and Evolution, 38(7), 3022-3027. https://dx.doi.org/10.1093/molbev/ msab120
  • Tufekci, E.F., Akcay, S., Kayipmaz, S., & Kiliç, A.O. (2019). Impact of quorum sensing inhibitors on population dynamics of oral bacteria. Journal of Biology, Agriculture and Healthcare, 9(18), 10-19. https://dx.doi.org/10.7176/JBAH
  • Velho-Pereira, S. & Kamat, N.M. (2011). Antimicrobial screening of actinobacteria using a modified cross-streak method. Indian Journal of Pharmaceutical Sciences, 73(2), 223-228. https://dx.doi.org/10.4103/ 0250-474x.91566
  • Yamaç, M., Işık, K., & Şahin, N. (2011). Numerical classifification of Streptomycetes isolated from karstic caves in Turkey. Turkish Journal of Biology, 35(4), 473-484. https://doi.org/10.3906/biy-0911-185
  • Yücel, S. & Yamaç, M. (2010). Selection of Streptomyces isolates from Turkish karstic caves against antibiotic resistant microorganisms. Pakistan Journal of Pharmaceutical Sciences, 23(1), 1–6.

Doğu Karadeniz Bölgesindeki Karstik Mağaralardan İzole Edilen Aktinomisetlerin Antimikrobiyal Aktivitelerinin ve 16S rRNA Dizilerinin Araştırılması

Yıl 2023, Cilt: 26 Sayı: 6, 1277 - 1290, 31.12.2023

Enis Fuat Tüfekci , Ümit Uzun , Nagihan Sağlam Ertunga , Ayşenur Biber , İnanç Alptuğ Hıdıroğlu , İlayda Tekkılıç , Birhan Altay , Ali Osman Kılıç

https://doi.org/10.18016/ksutarimdoga.vi.1226184
Cited By: 1

Öz

Günümüzde kullanılan antibiyotiklerin büyük çoğunluğunun başta Streptomyces cinsi olmak üzere çeşitli aktinomiset grubu bakterilerden orijin aldığı düşünüldüğünde, mağara gibi ekstrem ortamlardan izole edilecek yeni aktinomisetlerin tıp dünyasına yeni antibiyotikler kazandırabileceği öngörülmektedir. Bu çalışmada, üç farklı karstik mağaradan izole edilen aktinomiset izolatlarının antimikrobiyal aktivitelerinin araştırılması ve etkili izolatların moleküler yöntemlerle tanımlanması amaçlanmıştır. Çalışmaya Türkiye’nin Doğu Karadeniz Bölgesinde bulunan Gümüşhane ilindeki Akçakale, Kırklar (Altıntaş) ve Köprübaşı mağaralarından izole edilen 179 aktinomiset izolatı dahil edilmiştir. İzolatların antimikrobiyal aktiviteleri yedi Gram-negatif, üç Gram-pozitif ve bir maya suşuna karşı çapraz çizgi yöntemi ile araştırılmıştır. Elli üç izolatın (%29,6) test edilen mikroorganizmalardan en az birine karşı antimikrobiyal aktiviteye sahip olduğu bulunmuştur. İzolatların Staphylococcus aureus, Bacillus subtilis, Enterococcus faecalis, Chromobacterium violaceum, Klebsiella pneumoniae, Salmonella Typhimurium, Escherichia coli, Acinetobacter haemolyticus, Pseudomonas aeruginosa, Enterobacter aerogenes ve Candida albicans’a karşı antimikrobiyal aktivite sergileme oranı sırasıyla %21.2 %20.0, %16.8, %12.8, %3.4, %2.8, %2.2, %1.1, %0.6, %0.6, %0.6 şeklinde bulunmuştur. TRMS 124 olarak adlandırılan bir aktinomiset izolatı, 10 test mikroorganizmasına karşı antimikrobiyal aktivite sergilemiştir. En az üç test mikroorganizmasına karşı antimikrobiyal aktivite sergileyen aktinomisetler arasından randomize olarak seçilen 26 izolatın tanımlanması ve filogenetik analizi için 16S ribozomal RNA (16S rRNA) dizi analizi yapılmıştır. Buna göre 24 izolatın çeşitli Streptomyces türleri ile iki izolatın ise sırasıyla Embleya scabrispora ve Couchioplanes caeruleus ile homoloji gösterdiği tespit edilmiştir. Bu çalışmadan elde edilen bulgular karstik mağaraların antimikrobiyal madde üretme potansiyeline sahip aktinomisetlerin izolasyonu için doğal kaynaklar olabileceğini göstermiştir.

Anahtar Kelimeler

16S ribosomal RNA Actinomycetes Antimicrobial activity Cave Streptomyces

Destekleyen Kurum

Karadeniz Teknik Üniversitesi Bilimsel Araştırma Projeleri Koordinatörlüğü

Proje Numarası

FBA-2016-5481

Kaynakça

  • Alisjahbana, B., Debora, J., Susandi, E., & Darmawan, G. (2021). Chromobacterium violaceum: A review of an unexpected scourge. International Journal of General Medicine, 14, 3259-3270. https://doi.org/ 10.2147/IJGM.S272193
  • Bedel, H. (2020). Farklı Habitatlardan Toplanan Toprak ve Su Kaynaklarındaki Aktinomisetlerin İzolasyonu, Tanımlanmasi ve Antibakteriyel Aktivitenin Belirlenmesi (Tez No 663288). [Yüksek Lisans Tezi, Burdur Mehmet Akif Ersoy Üniversitesi Fen Bilimleri Enstitüsü Gıda Mühendisliği Ana Bilim Dalı]. Yükseköğretim Kurulu Ulusal Tez Merkezi.
  • Belyagoubi, L., Belyagoubi-Benhammou, N., Jurado, V., Dupont, J., Lacoste, S., Djebbah, F., Ounadjela, F.Z., Benaissa, S., Habi, S., Abdelouahi, D.E., & Saiz-Jimenez, C. (2018). Antimicrobial activities of culturable microorganisms (actinomycetes and fungi) isolated from Chaabe Cave, Algeria. International Journal of Speleology, 47(2), 189-199. https://doi.org/10.5038/1827-806X.47.2.2148
  • Cheeptham, N., Sadoway, T., Rule, D., Watson, K., Moote, P., Soliman, L.C., Azad, N., Donkor, K.K., & Horne, D. (2013). Cure from the cave: volcanic cave actinomycetes and their potential in drug discovery. International Journal of Speleology, 42(1), 35-47. http://dx.doi.org/10.5038/1827-806X.42.1.5
  • Chen, W.P. & Kuo, T.T. (1993). A simple and rapid method for the preparation of gram-negative bacterial genomic DNA. Nucleic acids research, 21(9), 2260. https://doi.org/10.1093/nar/21.9.2260
  • Devanshi, S., Shah, K.R., Arora, S. & Saxena, S. (2021). Actinomycetes as an environmental scrubber. In Abdel-Raouf, M.E., & El-Keshawy, M.H. (Eds.), Crude oil - new technologies and recent approaches. IntechOpen, London.
  • Doğruöz-Güngör, N., Çandıroğlu, B., & Altuğ, G. (2020). Enzyme profiles and antimicrobial activities of bacteria isolated from the Kadiini Cave, Alanya, Turkey. Journal of Cave and Karst Studies, 82(2), 106-115. https://doi.org/10.4311/2019MB0107
  • Farda, B., Djebaili, R., Vaccarelli, I., Del Gallo, M., & Pellegrini, M. (2022). Actinomycetes from caves: An overview of their diversity, biotechnological properties, and insights for their use in soil environments. Microorganisms, 10(2), 453. https:// doi.org/10.3390/microorganisms10020453
  • Farhana, A. & Khan, Y.S (2022). Biochemistry, Lipopolysaccharide. In: StatPearls [Internet]. Treasure Island (FL): StatPearls Publishing. Available from: https://www.ncbi.nlm.nih.gov/ books/NBK554414/ (Accessed on 1 May 2023).
  • Guo, Y., Zheng, W., Rong, X., & Huang, Y. (2008). A multilocus phylogeny of the Streptomyces griseus 16S rRNA gene clade: Use of multilocus sequence analysis for streptomycete systematics. International Journal of Systematic and Evolutionary Microbiology, 58(1), 149-159. https:// doi.org/10.1099/ijs.0.65224-0
  • Hamedi, J., Kafshnouchi, M., & Ranjbaran, M. (2019). A study on actinobacterial diversity of Hampoeil cave and screening of their biological activities. Saudi Journal of Biological Sciences, 26(7), 1587-1595. https://doi.org/10.1016/j.sjbs.2018.10.010
  • Herold, K., Gollmick, F.A., Groth, I., Roth, M., Menzel, K.D., Möllmann, U., Gräfe, U., & Hertweck, C. (2005). Cervimycin A-D: a polyketide glycoside complex from a cave bacterium can defeat vancomycin resistance. Chemistry (Weinheim an der Bergstrasse, Germany), 11(19), 5523-5530. https://doi.org/10.1002/chem.200500320
  • Hibbing, M.E., Fuqua, C., Parsek, M.R., & Peterson, S.B. (2010). Bacterial competition: surviving and thriving in the microbial jungle. Nature Reviews Microbiology, 8(1), 15-25. https://doi.org/10.1038/ nrmicro2259
  • Jaroszewicz, W., Bielańska, P., Lubomska, D., Kosznik-Kwaśnicka, K., Golec, P., Grabowski, Ł., Wieczerzak, E., Dróżdż, W., Gaffke, L., Pierzynowska, K., Węgrzyn, G., & Węgrzyn, A. (2021). Antibacterial, antifungal and anticancer activities of compounds produced by newly isolated Streptomyces strains from the Szczelina Chochołowska Cave (Tatra Mountains, Poland). Antibiotics (Basel, Switzerland), 10(10): 1212. https://doi.org/10.3390/antibiotics10101212
  • Kimura, M. (1980). A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution, 16(2), 111-120. https://doi.org/10.1007/BF01731581
  • Kováč, Ľ. (2018). Caves as oligotrophic ecosystems. In: Moldovan, O., Kováč, Ľ. & Halse, S. (Eds.), Cave ecology. Springer: Cham, Switzerland.
  • Labeda, D.P. (2011). Multilocus sequence analysis of phytopathogenic species of the genus Streptomyces. International Journal of Systematic and Evolutionary Microbiology, 61(10), 2525-2531. https://doi.org/10.1099/ijs.0.028514-0
  • Long, Y., Jiang, J., Hu, X., Zhou, J., Hu, J., & Zhou, S. (2019). Actinobacterial community in Shuanghe Cave using culture-dependent and -independent approaches. World Journal of Microbiology & Biotechnology, 35(10), 153. https://doi.org/ 10.1007/ s11274-019-2713-y
  • Maciejewska, M., Adam, D., Martinet, L., Naômé, A., Całusińska, M., Delfosse, P., Carnol, M., Barton, H. A., Hayette, M. P., Smargiasso, N., De Pauw, E., Hanikenne, M., Baurain, D., & Rigali, S. (2016). A phenotypic and genotypic analysis of the antimicrobial potential of cultivable Streptomyces isolated from cave moonmilk deposits. Frontiers in Microbiology, 7,1455. https://doi.org/10.3389/ fmicb.2016.01455
  • Miethke, M., Pieroni, M., Weber, T., Brönstrup, M., Hammann, P., Halby, L., Arimondo, P.B., Glaser, P., Aigle, B., Bode, H.B., Moreira, R., Li, Y., Luzhetskyy, A., Medema, M.H., Pernodet, J.L., Stadler, M., Tormo, J.R., Genilloud, O., Truman, A.W., … Müller, R. (2021). Towards the sustainable discovery and development of new antibiotics. Nature Reviews Chemistry, 5(10), 726-749. https://doi.org/10.1038/s41570-021-00313-1
  • Nimaichand, S., Devi, A.M., Tamreihao, K., Ningthoujam, D.S., & Li, W.J. (2015). Actinobacterial diversity in limestone deposit sites in Hundung, Manipur (India) and their antimicrobial activities. Frontiers in Microbiology, 6, 413. https://doi.org/10.3389/fmicb.2015.00413
  • Pradana, A.D., Sekarini, D.N., Suma, A.A., & Maliza, R. (2022). Study on the antibacterial effect from moonmilk Pindul Cave, Indonesia. Iranian Journal of Medical Microbiology, 16(2), 165-172. https://doi.org/10.30699/ijmm.16.2.165
  • Procópio, R.E., Silva, I.R., Martins, M.K., Azevedo, J.L., & Araújo, J.M. (2012). Antibiotics produced by Streptomyces. The Brazilian journal of infectious diseases: an official publication of the Brazilian Society of Infectious Diseases, 16(5), 466-471. https://dx.doi.org/10.1016/j.bjid.2012.08.014
  • Prudence, S.M.M., Addington, E., Castaño-Espriu, L., Mark, D.R., Pintor-Escobar, L., Russell, A.H., & McLean, T.C. (2020). Advances in actinomycete research: An ActinoBase review of 2019. Microbiology (Reading, England), 166(8), 683-694. https://dx.doi.org/10.1099/mic.0.000944
  • Rangseekaew, P. & Pathom-Aree, W. (2019). Cave actinobacteria as producers of bioactive metabolites. Frontiers in Microbiology, 10, 387. https://dx.doi.org/10.3389/fmicb.2019.00387
  • Rong, X. & Huang, Y. (2012). Taxonomic evaluation of the Streptomyces hygroscopicus clade using multilocus sequence analysis and DNA-DNA hybridization, validating the MLSA scheme for systematics of the whole genus. Systematic and Applied Microbiology, 35(1), 7-18. https://dx.doi.org/ 10.1016/j.syapm.2011.10.004
  • Saitou, N. & Nei, M. (1987). The neighbor-joining method: a new method for reconstructing phylogenetic trees. Molecular Biology and Evolution, 4(4), 406-425. https://dx.doi.org/10.1093/ oxfordjournals.molbev.a040454
  • Selim, M.S.M., Abdelhamid, S.A., & Mohamed, S.S. (2021). Secondary metabolites and biodiversity of actinomycetes. Journal, Genetic Engineering & Biotechnology, 19(1), 72. https://doi.org/10.1186/ s43141-021-00156-9
  • SPSS, (2015). IBM SPSS Statistics 23.0 for Windows. Armonk, NY.
  • Syiemiong, D. & Jha, D.K. (2019). Antibacterial potential of actinobacteria from a limestone mining site in Meghalaya, India. Journal of Pure and Applied Microbiology, 13(2), 789-802. https:// dx.doi.org/10.22207/JPAM.13.2.14
  • Tamura, K., Stecher, G., & Kumar, S. (2021). MEGA 11: Molecular evolutionary genetics analysis version 11. Molecular Biology and Evolution, 38(7), 3022-3027. https://dx.doi.org/10.1093/molbev/ msab120
  • Tufekci, E.F., Akcay, S., Kayipmaz, S., & Kiliç, A.O. (2019). Impact of quorum sensing inhibitors on population dynamics of oral bacteria. Journal of Biology, Agriculture and Healthcare, 9(18), 10-19. https://dx.doi.org/10.7176/JBAH
  • Velho-Pereira, S. & Kamat, N.M. (2011). Antimicrobial screening of actinobacteria using a modified cross-streak method. Indian Journal of Pharmaceutical Sciences, 73(2), 223-228. https://dx.doi.org/10.4103/ 0250-474x.91566
  • Yamaç, M., Işık, K., & Şahin, N. (2011). Numerical classifification of Streptomycetes isolated from karstic caves in Turkey. Turkish Journal of Biology, 35(4), 473-484. https://doi.org/10.3906/biy-0911-185
  • Yücel, S. & Yamaç, M. (2010). Selection of Streptomyces isolates from Turkish karstic caves against antibiotic resistant microorganisms. Pakistan Journal of Pharmaceutical Sciences, 23(1), 1–6.
Toplam 35 adet kaynakça vardır.

Ayrıntılar

Birincil Dil İngilizce
Konular Mikrobiyoloji (Diğer)
Bölüm ARAŞTIRMA MAKALESİ (Research Article)
Yazarlar

Enis Fuat Tüfekci 0000-0001-5051-2694

Ümit Uzun 0000-0002-0585-2865

Nagihan Sağlam Ertunga 0000-0002-2104-2192

Ayşenur Biber 0000-0001-8431-2703

İnanç Alptuğ Hıdıroğlu 0000-0002-3030-6006

İlayda Tekkılıç 0000-0002-2522-7370

Birhan Altay 0000-0003-2025-7869

Ali Osman Kılıç 0000-0002-5506-0866

Proje Numarası FBA-2016-5481
Erken Görünüm Tarihi 14 Haziran 2023
Yayımlanma Tarihi 31 Aralık 2023
Gönderilme Tarihi 31 Aralık 2022
Kabul Tarihi 8 Mayıs 2023
Yayımlandığı Sayı Yıl 2023 Cilt: 26 Sayı: 6

Kaynak Göster

APA Tüfekci, E. F., Uzun, Ü., Sağlam Ertunga, N., … Biber, A. (2023). Investigation of Antimicrobial Activities and 16S rRNA Sequences of Actinomycetes Isolated from Karst Caves in the Eastern Black Sea Region of Türkiye. Kahramanmaraş Sütçü İmam Üniversitesi Tarım ve Doğa Dergisi, 26(6), 1277-1290. https://doi.org/10.18016/ksutarimdoga.vi.1226184

Cited By

Taxonomic characterization and secondary metabolite production of newly isolated Streptomyces sp. MC12
International Journal of Secondary Metabolite
https://doi.org/10.21448/ijsm.1481362
 Kapak Resmi İndir

21082



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2022-JCI = 0.170

Uluslararası Hakemli Dergi (International Peer Reviewed Journal)

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      Yılda 6 sayı yayınlanır. (Published 6 times a year)


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