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Laktik asit bakterilerinde çoğunluğu algılama mekanizması

Year 2015, Volume: 72 Issue: 1, 79 - 90, 01.03.2015

Abstract

Uzun yıllar mikroorganizmaların sadece çoğalan, besin arayan kendi başlarına yaşayan hücreler oldukları düşünülmüştür. Ancak 50 yıl önce mikrobiyologlar tarafından bakterilerin birbirleri ve çevreleri ile iletişim kurduklarının dünyasına bakış açısı değişmiştir. İletişimde kullanılan dil, sinyal moleküllerinden oluşmakta ve sinyal moleküllerine genel olarak “otoindükleyici” adı verilmektedir. Bakteriler üretilen sinyal moleküllerinin yoğunluğunu ölçebilmekte, bu sayede ortamdaki diğer mikroorganizmaların miktarını algılayabilmekte ve türe özgü davranışlar sergileyebilmektedirler. Yapılan çalışmalar; farklı mikroorganizmaların farklı çoğunluğu algılama ÇA moleküllerini kullandıklarını, hatta bazı mikroorganizmaların bir kaç çeşit sinyal molekülünü birden kullandığını ortaya koymuştur. LuxI/LuxR sistemi, oligopeptit sistemi ve hibrit sistem olmak üzere üç çeşit çoğunluğu algılama mekanizması tanımlanmıştır. Bu mekanizmalarda kullanılan sinyal molekülü ve bu molekülün algılanması birbirinden farklıdır. Çoğunluğu algılama ile ilgili ilk çalışmalar deniz suyunda yaşayan Vibrio fischeri ve Vibrio harveyi bakterileri üzerinde yapılmış ve sonraki aşamada patojen bakteriler üzerine yoğunlaşmıştır. Spor oluşturma, konjugasyan, biyolüminesans, biyofilm oluşturma, antibiyotik üretimi ve bakteriyosin üretimi gibi türe özgü pek çok davranış ÇA mekanizması ile kontrol edilmektedir. ÇA mekanizmasının anlaşılması, patojen mikroorganizmalarla etkili şekilde mücadele edilmesinde ve laktik asit bakterilerinin davranışlarının anlaşılmasında son derece önemlidir. Ancak laktik asit bakterilerinin ÇA mekanizmasının çok farklı sinyal moleküllerinin kullanılması ve algılamanın olaylar dizisi şeklinde gerçekleşmesi nedeniyle anlaşılması zordur. Bu derlemede, sağlık üzerine olumlu katkı sağlayan probiyotik özellikteki laktik asit bakterilerinin konakçısı ile uyumu, sindirim sistemindeki patojenlerin gelişimini ve koloni oluşturmasını engellemesi, bakteriyosin üretimi, asit koşullara ve safra tuzlarına dayanımı, epitel hücrelere tutunma gibi pek çok özelliğinin ÇA ile bağlantısı değerlendirilmiştir. Laktik asit bakterileri tarafından kullanılan ÇA mekanizmasının anlaşılması ile yeni dönem probiyotikler olarak tanımlanan metabiyotiklerin tasarlanmasında yarar sağlayacağı düşünülmektedir

References

  • Gobbetti M, De Angelis M, Di Cagno R, Minervini F, Limitone A. Cell–cell communication in food related bacteria. Int J Food Microbiol, 2007; 120, 34–45.
  • Bassler BL. How bacteria talk to each other: regulation of gene expression by quorum sensing. Curr Opin Microbiol, 1999; 2, 582–87.
  • Saraçlı MA. "Quorum sensing": mikroorganizmalar iletişim mi kuruyor? Gülhane Tıp Derg, 2006; 48, 244-50.
  • Smid EJ, Lacroix C. Microbe–microbe interactions in mixed culture food fermentations. Curr Opin Biotechnol, 2013; 24: 148–54.
  • Daniels R, Vanderleyden J, Michiels J. Quorum sensing and swarming migration in bacteria. FEMS Microbiol Rev, 2004; 28: 261–89.
  • Schauder S, Bassler BL. The languages of bacteria. Genes Dev, 2001; 15: 1468-80.
  • Eriş R. Gül (Rosa damascena mill.) yağı, absolütü ve gül suyunun Chromobacterium violaceum ATCC 12472, CV026 ve CVIR 07 suşlarının çevreyi algılama sistemleri (quorum sensing) üzerine etkisinin araştırılması. Yüksek Lisans Tezi, Süleyman Demirel Üniversitesi, Fen Bilimleri Enstitüsü, 2011.
  • Miller MB, Bassler BL. Quorum sensing in bacteria. Annu Rev Microbiol, 2001; 55: 165-99.
  • Avcı MK. Quorum sensing odaklı yenilikler ve biyoteknolojik uygulamalar. MBG 617 Bbiyoteknolojide quorumsensing.net, 2009. gelişmeler, www.
  • LaSarre B, Federle MJ. Exploiting quorum sensing to confuse bacterial pathogens. Microbiol Mol Biol Rev, 2013; 77 (1): 73.
  • Kleerebezem M, Quadri LEN, Kuipers OP, de Vos WM. Quorum sensing by peptide pheromones and two- component signal transduction systems in Gram- positive bacteria. Mol Microbiol, 1997; 24 (5): 895- 904.
  • Xavier KB, Bassler BL. LuxS quorum sensing: more than just a numbers game. Curr Opin Microbiol, 2003; 6: 191–97.
  • Abee T, Kovacs AT, Kuipers OP, van der Veen S. Biofilm formation and dispersal in Gram-positive bacteria. Curr Opin Biotechnol, 2011; 22: 172–79.
  • Jaraman A, Wood TK. Bacterial quorum sensing: signals, circuits, and implications for biofilms and disease. Annu Rev Biomed Eng, 2008; 10: 145-67.
  • Winzer K, Hardie KR, Burgess N. LuxS: its role in central metabolism and the in vitro synthesis of 4-hydroxy- 5-methyl-3(2H)-furanone. J Gen Microbiol, 2002; 148: 909-22.
  • Shiner EK, Rumbaugh KP, Williams SC. Interkingdom signalling: the language of acylhomoserine lactones. FEMS Microbiol Rev, 2005; 29: 935-47.
  • Di Cagno R, De Angelis M, Calasa M, Gobbetti M. Proteomics of the bacterial cross-talk by quorum sensing. J Proteomics, 2011; 74: 19-34.
  • Baskın H. İnsan florası ve “quorum sensing”. Klimik 13. Türk Klinik Mikrobiyoloji ve İnfeksiyon Hastalıkları Kongresi, Mart, 23-27, Antalya- Türkiye. 2007.
  • Hayes SH, Low DA. Signals of growth regulation in bacteria. Curr Opin Microbiol, 2009; 12: 667–73.
  • Simoes M, Simoes L.C, Vieira M.J. A review of current and emergent biofilm control strategies. Lebenson Wiss Technol, 2010; 43: 573–83.
  • Lazar V. Quorum sensing in biofilms - How to destroy the bacterial citadels or their cohesion/ power? Anaerobe, 2011; 17: 280-285.
  • Oppenheimer-Shaanan Y, Steinberg N, Kolodkin- Gal I. Small molecules are natural triggers for the disassembly of biofilms. Trends Microbiol, 2013; 21(11): 591-601.
  • Sifri CD. Quorum sensing: Bacteria talk sense. Clin Infect Dis, 2008; 47: 1070–6.
  • Mc.Gowan SJ, Barnard AM, Boşgelmez G, Sebaihia M, Simpson NJ, Thomson NR, et al. Carbepenem antibiotic biosynthesis in Erwinia carotovora is regulated by physcological and genetic factors modulating the quorum sensing-depent control pathway. Mol Microbiol, 2005; 2: 526-45.
  • Kleerebezem M. Quorum sensing control of lantibiotic production; nisin and subtilin autoregulate their own biosynthesis. Peptides, 2004; 25: 1405–14.
  • Lebeer S, Vanderleyden J, De Keersmaecker SCJ. Genes and molecules of lactobacilli supporting probiotic action. Microbiol Mol Biol Rev, 2008; 72: 728–64.
  • Dobson A, Cotter PD, Ross RP, Hill C. Bacteriocin production: a probiotic trait?. Appl Environ Microbiol, 2012; 78(1): 1-6.
  • Carey CM, Kostrzynska M, Thompson S. Escherichia coli O157:H7 stress and virulence gene expression on Romaine lettuce using comparative real-time PCR. J Microbiol Methods, 2009; 77: 235–42.
  • Tong Z, Zhou L, Li J, Kuang R, Lin Y, Ni L. An in vitro investigation of Lactococcus lactis antagonizing cariogenic bacterium Streptococcus mutans. Arch Oral Biol, 2012; 57: 376-82.
  • Karatuna O, Yağcı A. Pseudomonas aeruginosa’da virülans faktörleri ve quorum sensing. Turk Mikrobiyol Cemiy Derg, 2008; 38(1): 42-51.
  • Donabedian H. Quorum sensing and its relevance to infectious diseases. J Infect, 2003; 46: 207-14.
  • Karaman M, Yılmaz O, Bayrakal V, Bahar İH. Gentamisin ve imipenem etkisinde Pseudomonas aeruginosa quorum sensing yanıtları ve biyofilm üretimi: In-vivo modelleme. ANKEM, 2010; 24(2): 76-81.
  • Çakır İ, Karahan AG, Çakmakçı ML. Probiyotikler ve etki mekanizmaları. Gıda Müh Derg, 2002; 6 (12): 15-9.
  • Schroeter J, Klaenhammer T. Genomics of lactic acid bacteria. FEMS Microbiol Lett, 2009; 292: 1–6.
  • Shenderov BA. Probiotic (symbiotic) bacterial languages. Anaerobe, 2011; 1: 490-5.
  • O’Flaherty S, Klaenhammer TR. The role and potential of probiotic bacteria in the gut, and the communication between gut microflora and gut/ host. Int Dairy J, 2010; 20: 262–8.
  • Pfeiler EA, Azcarate-Peril MA, Klaenhammer TR. Characterization of a novel bile-inducible operon encoding a two-component regulatory system in Lactobacillus acidophilus. J Bacteriol, 2007; 189: 4624–34.
  • Moslehi-Jenabian S, Gori K, Jespersen L. AI-2 signalling is induced by acidic shock in probiotic strains of Lactobacillus spp.. Int J Food Microbiol, 2009; 135: 295–302.
  • Zhou XX, Li WF, Ma GX, Pan YJ. The nisin- controlled gene expression system: Construction, application and improvements. Biotechnol Adv, 2006; 24: 285– 95.
  • Navarro L, Rojo-Bezares B, Sáenz Y, Díez L, Zarazaga M, Ruiz-Larrea F, et al. Comparative study of the pln locus of the quorum-sensing regulated bacteriocinproducing. L. plantarum J51 strain. Int J Food Microbiol, 2008; 128: 390–4.
  • Diep DB, Straume D, Kjos M, Torres C, Nes I. An overview of the mosaic bacteriocin pln loci from Lactobacillus plantarum. Peptides, 2009; 30: 1562–74.
  • Man LL, Meng XC, Zhao RH. Induction of plantaricin MG under co-culture with certain lactic acid bacterial strains and identification of LuxS mediated quorum sensing system in Lactobacillus plantarum KLDS1.0391. Food Control, 2012; 23: 462-9.
  • Bauer R, du Toit M, Kossmann J. Influence of environmental parameters on production of the acrolein precursor 3-hydroxypropionaldehyde by Lactobacillus reuteri DSMZ 20016 and its accumulation by wine lactobacilli. Int J Food Microbiol, 2010; 137: 28–31.
  • Karahan AG, Çakmakçı ML. Determination of some properties of Lactobacillus strains isolated from cecum. J Agri Sci, 1998; 4: 59-64.
  • Moslehi-Jenabian S, Vogensen FK, Jespersen L. The quorum sensing luxS gene is induced in Lactobacillus acidophilus NCFM in response to Listeria monocytogenes. Int J Food Microbiol, 2011; 149: 269–73.
  • Tabasco R, de Palencia PF, Fontecha Peláez C, Requena T. Competition mechanisms of lactic acid bacteria and bifidobacteria: fermentative metabolism and colonization. LWT – Food Sci Technol, 2014; 55: 680-4.
  • Chu W, Lu F, Zhu W, Kang C. Isolation and characterization of new potential probiotic bacteria based on quorum-sensing system. J Appl Microbiol, 2010; 110: 202–8.
  • Kalia VC. Quorum sensing inhibitors: an overview. Biotechnol Adv, 2013; 31: 224–45.
  • Tuan TN, Duc PM, Hatai K. Overview of the use of probiotics in aquaculture. Int J Res Fish Aquac, 2013; 3(3): 89-97.
  • Cotar AI. Quorum sensing inhibitors as anti- pathogenic drugs in the fight against Pseudomonas aeruginosa infections. Clin Microbiol, 2013; 2(4): 1-2.
  • Lenz CA, Hew Ferstl CM, Vogel RF. Sub-lethal stress effects on virulence gene expression in Enterococcus faecalis. Food Microbiol, 2010; 27: 317-26.

Quorum sensing mechanism in lactic acid bacteria

Year 2015, Volume: 72 Issue: 1, 79 - 90, 01.03.2015

Abstract

For a long time, microorganisms were considered as just multiplying, finding nutrients and living by themselves organisms. But that belief changed 50 years ago along with the discovery of bacteria communication with each other and environment by microbiologists. The language used in the communication consists of signal molecules and these molecules are generally called “auto inducer”. Bacteria are capable of measuring density of these molecules and by this way they are able to detect amount of the other organisms and can have specific behaviors. Studies prove that different types of bacteria use different quorum sensing molecules, and some species use several kinds of signal molecules together. There are three described quorum sensing mechanisms; LuxI/LuxR, oligopeptide and hybrid system. Among these systems, type of signal molecules and their perceptions are different from each other. The first quorum sensing studies are accomplished on Vibrio fischeri and Vibrio harveyi and then focused on pathogen microorganisms. Many specific behaviors such as spore forming, conjugation, bioluminescense, biofilm forming, antibiotic production and bacteriocin production are controlled by quorum sensing mechanisms. Understanding of QS mechanism is very important in the terms of effective struggling with pathogen microorganisms and understanding behavior of lactic acid bacteria. Because of lactic acid bacteria use different type of signal molecules and detection occurs as a consecution it is hard to understand their QS mechanism. In this review, connection between QS mechanism and some characteristics of lactic acid bacteria are evaluated such as concordance with its host, inhibition of pathogen development and colonization in gastrointestinal system, bacteriocin production, acid and bile resistance, adhesion to epithelium cells. Understanding QS mechanism of lactic acid bacteria will be useful to design metabiotics which is defined as novel probiotics.

References

  • Gobbetti M, De Angelis M, Di Cagno R, Minervini F, Limitone A. Cell–cell communication in food related bacteria. Int J Food Microbiol, 2007; 120, 34–45.
  • Bassler BL. How bacteria talk to each other: regulation of gene expression by quorum sensing. Curr Opin Microbiol, 1999; 2, 582–87.
  • Saraçlı MA. "Quorum sensing": mikroorganizmalar iletişim mi kuruyor? Gülhane Tıp Derg, 2006; 48, 244-50.
  • Smid EJ, Lacroix C. Microbe–microbe interactions in mixed culture food fermentations. Curr Opin Biotechnol, 2013; 24: 148–54.
  • Daniels R, Vanderleyden J, Michiels J. Quorum sensing and swarming migration in bacteria. FEMS Microbiol Rev, 2004; 28: 261–89.
  • Schauder S, Bassler BL. The languages of bacteria. Genes Dev, 2001; 15: 1468-80.
  • Eriş R. Gül (Rosa damascena mill.) yağı, absolütü ve gül suyunun Chromobacterium violaceum ATCC 12472, CV026 ve CVIR 07 suşlarının çevreyi algılama sistemleri (quorum sensing) üzerine etkisinin araştırılması. Yüksek Lisans Tezi, Süleyman Demirel Üniversitesi, Fen Bilimleri Enstitüsü, 2011.
  • Miller MB, Bassler BL. Quorum sensing in bacteria. Annu Rev Microbiol, 2001; 55: 165-99.
  • Avcı MK. Quorum sensing odaklı yenilikler ve biyoteknolojik uygulamalar. MBG 617 Bbiyoteknolojide quorumsensing.net, 2009. gelişmeler, www.
  • LaSarre B, Federle MJ. Exploiting quorum sensing to confuse bacterial pathogens. Microbiol Mol Biol Rev, 2013; 77 (1): 73.
  • Kleerebezem M, Quadri LEN, Kuipers OP, de Vos WM. Quorum sensing by peptide pheromones and two- component signal transduction systems in Gram- positive bacteria. Mol Microbiol, 1997; 24 (5): 895- 904.
  • Xavier KB, Bassler BL. LuxS quorum sensing: more than just a numbers game. Curr Opin Microbiol, 2003; 6: 191–97.
  • Abee T, Kovacs AT, Kuipers OP, van der Veen S. Biofilm formation and dispersal in Gram-positive bacteria. Curr Opin Biotechnol, 2011; 22: 172–79.
  • Jaraman A, Wood TK. Bacterial quorum sensing: signals, circuits, and implications for biofilms and disease. Annu Rev Biomed Eng, 2008; 10: 145-67.
  • Winzer K, Hardie KR, Burgess N. LuxS: its role in central metabolism and the in vitro synthesis of 4-hydroxy- 5-methyl-3(2H)-furanone. J Gen Microbiol, 2002; 148: 909-22.
  • Shiner EK, Rumbaugh KP, Williams SC. Interkingdom signalling: the language of acylhomoserine lactones. FEMS Microbiol Rev, 2005; 29: 935-47.
  • Di Cagno R, De Angelis M, Calasa M, Gobbetti M. Proteomics of the bacterial cross-talk by quorum sensing. J Proteomics, 2011; 74: 19-34.
  • Baskın H. İnsan florası ve “quorum sensing”. Klimik 13. Türk Klinik Mikrobiyoloji ve İnfeksiyon Hastalıkları Kongresi, Mart, 23-27, Antalya- Türkiye. 2007.
  • Hayes SH, Low DA. Signals of growth regulation in bacteria. Curr Opin Microbiol, 2009; 12: 667–73.
  • Simoes M, Simoes L.C, Vieira M.J. A review of current and emergent biofilm control strategies. Lebenson Wiss Technol, 2010; 43: 573–83.
  • Lazar V. Quorum sensing in biofilms - How to destroy the bacterial citadels or their cohesion/ power? Anaerobe, 2011; 17: 280-285.
  • Oppenheimer-Shaanan Y, Steinberg N, Kolodkin- Gal I. Small molecules are natural triggers for the disassembly of biofilms. Trends Microbiol, 2013; 21(11): 591-601.
  • Sifri CD. Quorum sensing: Bacteria talk sense. Clin Infect Dis, 2008; 47: 1070–6.
  • Mc.Gowan SJ, Barnard AM, Boşgelmez G, Sebaihia M, Simpson NJ, Thomson NR, et al. Carbepenem antibiotic biosynthesis in Erwinia carotovora is regulated by physcological and genetic factors modulating the quorum sensing-depent control pathway. Mol Microbiol, 2005; 2: 526-45.
  • Kleerebezem M. Quorum sensing control of lantibiotic production; nisin and subtilin autoregulate their own biosynthesis. Peptides, 2004; 25: 1405–14.
  • Lebeer S, Vanderleyden J, De Keersmaecker SCJ. Genes and molecules of lactobacilli supporting probiotic action. Microbiol Mol Biol Rev, 2008; 72: 728–64.
  • Dobson A, Cotter PD, Ross RP, Hill C. Bacteriocin production: a probiotic trait?. Appl Environ Microbiol, 2012; 78(1): 1-6.
  • Carey CM, Kostrzynska M, Thompson S. Escherichia coli O157:H7 stress and virulence gene expression on Romaine lettuce using comparative real-time PCR. J Microbiol Methods, 2009; 77: 235–42.
  • Tong Z, Zhou L, Li J, Kuang R, Lin Y, Ni L. An in vitro investigation of Lactococcus lactis antagonizing cariogenic bacterium Streptococcus mutans. Arch Oral Biol, 2012; 57: 376-82.
  • Karatuna O, Yağcı A. Pseudomonas aeruginosa’da virülans faktörleri ve quorum sensing. Turk Mikrobiyol Cemiy Derg, 2008; 38(1): 42-51.
  • Donabedian H. Quorum sensing and its relevance to infectious diseases. J Infect, 2003; 46: 207-14.
  • Karaman M, Yılmaz O, Bayrakal V, Bahar İH. Gentamisin ve imipenem etkisinde Pseudomonas aeruginosa quorum sensing yanıtları ve biyofilm üretimi: In-vivo modelleme. ANKEM, 2010; 24(2): 76-81.
  • Çakır İ, Karahan AG, Çakmakçı ML. Probiyotikler ve etki mekanizmaları. Gıda Müh Derg, 2002; 6 (12): 15-9.
  • Schroeter J, Klaenhammer T. Genomics of lactic acid bacteria. FEMS Microbiol Lett, 2009; 292: 1–6.
  • Shenderov BA. Probiotic (symbiotic) bacterial languages. Anaerobe, 2011; 1: 490-5.
  • O’Flaherty S, Klaenhammer TR. The role and potential of probiotic bacteria in the gut, and the communication between gut microflora and gut/ host. Int Dairy J, 2010; 20: 262–8.
  • Pfeiler EA, Azcarate-Peril MA, Klaenhammer TR. Characterization of a novel bile-inducible operon encoding a two-component regulatory system in Lactobacillus acidophilus. J Bacteriol, 2007; 189: 4624–34.
  • Moslehi-Jenabian S, Gori K, Jespersen L. AI-2 signalling is induced by acidic shock in probiotic strains of Lactobacillus spp.. Int J Food Microbiol, 2009; 135: 295–302.
  • Zhou XX, Li WF, Ma GX, Pan YJ. The nisin- controlled gene expression system: Construction, application and improvements. Biotechnol Adv, 2006; 24: 285– 95.
  • Navarro L, Rojo-Bezares B, Sáenz Y, Díez L, Zarazaga M, Ruiz-Larrea F, et al. Comparative study of the pln locus of the quorum-sensing regulated bacteriocinproducing. L. plantarum J51 strain. Int J Food Microbiol, 2008; 128: 390–4.
  • Diep DB, Straume D, Kjos M, Torres C, Nes I. An overview of the mosaic bacteriocin pln loci from Lactobacillus plantarum. Peptides, 2009; 30: 1562–74.
  • Man LL, Meng XC, Zhao RH. Induction of plantaricin MG under co-culture with certain lactic acid bacterial strains and identification of LuxS mediated quorum sensing system in Lactobacillus plantarum KLDS1.0391. Food Control, 2012; 23: 462-9.
  • Bauer R, du Toit M, Kossmann J. Influence of environmental parameters on production of the acrolein precursor 3-hydroxypropionaldehyde by Lactobacillus reuteri DSMZ 20016 and its accumulation by wine lactobacilli. Int J Food Microbiol, 2010; 137: 28–31.
  • Karahan AG, Çakmakçı ML. Determination of some properties of Lactobacillus strains isolated from cecum. J Agri Sci, 1998; 4: 59-64.
  • Moslehi-Jenabian S, Vogensen FK, Jespersen L. The quorum sensing luxS gene is induced in Lactobacillus acidophilus NCFM in response to Listeria monocytogenes. Int J Food Microbiol, 2011; 149: 269–73.
  • Tabasco R, de Palencia PF, Fontecha Peláez C, Requena T. Competition mechanisms of lactic acid bacteria and bifidobacteria: fermentative metabolism and colonization. LWT – Food Sci Technol, 2014; 55: 680-4.
  • Chu W, Lu F, Zhu W, Kang C. Isolation and characterization of new potential probiotic bacteria based on quorum-sensing system. J Appl Microbiol, 2010; 110: 202–8.
  • Kalia VC. Quorum sensing inhibitors: an overview. Biotechnol Adv, 2013; 31: 224–45.
  • Tuan TN, Duc PM, Hatai K. Overview of the use of probiotics in aquaculture. Int J Res Fish Aquac, 2013; 3(3): 89-97.
  • Cotar AI. Quorum sensing inhibitors as anti- pathogenic drugs in the fight against Pseudomonas aeruginosa infections. Clin Microbiol, 2013; 2(4): 1-2.
  • Lenz CA, Hew Ferstl CM, Vogel RF. Sub-lethal stress effects on virulence gene expression in Enterococcus faecalis. Food Microbiol, 2010; 27: 317-26.
There are 51 citations in total.

Details

Primary Language Turkish
Journal Section Research Article
Authors

Hatice Yılmaz -yıldıran This is me

Aynur Gül Karahan This is me

Gülden Başyiğit -kılıç This is me

Publication Date March 1, 2015
Published in Issue Year 2015 Volume: 72 Issue: 1

Cite

APA Yılmaz -yıldıran, H., Karahan, A. G., & Başyiğit -kılıç, G. (2015). Laktik asit bakterilerinde çoğunluğu algılama mekanizması. Türk Hijyen Ve Deneysel Biyoloji Dergisi, 72(1), 79-90.
AMA Yılmaz -yıldıran H, Karahan AG, Başyiğit -kılıç G. Laktik asit bakterilerinde çoğunluğu algılama mekanizması. Turk Hij Den Biyol Derg. March 2015;72(1):79-90.
Chicago Yılmaz -yıldıran, Hatice, Aynur Gül Karahan, and Gülden Başyiğit -kılıç. “Laktik Asit Bakterilerinde çoğunluğu algılama Mekanizması”. Türk Hijyen Ve Deneysel Biyoloji Dergisi 72, no. 1 (March 2015): 79-90.
EndNote Yılmaz -yıldıran H, Karahan AG, Başyiğit -kılıç G (March 1, 2015) Laktik asit bakterilerinde çoğunluğu algılama mekanizması. Türk Hijyen ve Deneysel Biyoloji Dergisi 72 1 79–90.
IEEE H. Yılmaz -yıldıran, A. G. Karahan, and G. Başyiğit -kılıç, “Laktik asit bakterilerinde çoğunluğu algılama mekanizması”, Turk Hij Den Biyol Derg, vol. 72, no. 1, pp. 79–90, 2015.
ISNAD Yılmaz -yıldıran, Hatice et al. “Laktik Asit Bakterilerinde çoğunluğu algılama Mekanizması”. Türk Hijyen ve Deneysel Biyoloji Dergisi 72/1 (March 2015), 79-90.
JAMA Yılmaz -yıldıran H, Karahan AG, Başyiğit -kılıç G. Laktik asit bakterilerinde çoğunluğu algılama mekanizması. Turk Hij Den Biyol Derg. 2015;72:79–90.
MLA Yılmaz -yıldıran, Hatice et al. “Laktik Asit Bakterilerinde çoğunluğu algılama Mekanizması”. Türk Hijyen Ve Deneysel Biyoloji Dergisi, vol. 72, no. 1, 2015, pp. 79-90.
Vancouver Yılmaz -yıldıran H, Karahan AG, Başyiğit -kılıç G. Laktik asit bakterilerinde çoğunluğu algılama mekanizması. Turk Hij Den Biyol Derg. 2015;72(1):79-90.