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ÇEŞİTLİ SUCUL HİPERSALİN HABİTATLARDAKİ (TÜRKİYE) PROKARYOTİK TOPLULUKLARIN VE NANOHALOARKEAL SOYLARIN ÇEŞİTLİLİĞİNİN YÜKSEK-VERİMLİ DİZİLEME VE KLONLAMA KULLANILARAK DEĞERLENDİRİLMESİ

Yıl 2021, Cilt: 10 Sayı: 1, 57 - 68, 25.01.2021
https://doi.org/10.18036/estubtdc.777824

Öz

Bu çalışmada, 16S rRNA geni hedefli yaklaşımlar kullanılarak prokaryotik grupların Tuz Gölü, Ayvalık ve Tuzlagözü güneş tuzlalarındaki dağılımı araştırılmıştır. Numunelerdeki prokaryotik taksonların nispi bolluğu, yüksek-verimli dizileme kullanılarak saptanmıştır. Haloquadratum ile ilişkili operasyonel taksonomik birimler (OTU'lar) MiSeq okumalarında en bol saptananlardı. Nanohaloarchaeota-ilişkili OTU’lar Ayvalık ve Tuzlagözü güneş tuzlalarında nadirdi (<%1), ve Tuz Gölü'nde yaklaşık %5 idi. Örneklerde sıklıkla bulunan ve paylaşılan diğer OTU'lar Halorubrum, Halonotius ve Salinibacter cinsleri ile ilişkiliydi.

Filotipleri çeşitli hipersalin ortamlarda sıklıkla tespit edilen Nanohaloarchaeota soyları, gruba özgü primer kullanılarak 16S rRNA gen klonlama ile daha ayrıntılı olarak incelenmiştir. Klon kütüphanelerinde yüksek oranda temsil edilen nanohaloarkeal filotiplerden bazıları, veri tabanındaki dizilere düşük benzerlik göstererek iki farklı dal oluşturmuştur. Ayvalık örneğinden oluşturulan klon kütüphanesinde yeni soylardan birinin öne çıktığı saptanmıştır. Ca. Nanopetramus'a % 95-97 dizi benzerliği gösteren filotipler de Ayvalık’ta yüksek oranda temsil edilmiştir. Tuz Gölü ve Tuzlagözü numunelerinin klon kütüphanelerinde sıklıkla saptanan filotipler, Ca. Nanosalina ve akrabalarının yanı sıra yeni bir soy ile ilişkilendirilmiştir.

Kaynakça

  • [1] Antón J, Llobet‐Brossa E, Rodríguez‐Valera F, Amann R. Fluorescence in situ hybridization analysis of the prokaryotic community inhabiting crystallizer ponds. Environ Microbiol 1999; 1:517-523.
  • [2] Baati H, Guermazi S, Amdouni R, Gharsallah N, Sghir A, Ammar E. Prokaryotic diversity of a Tunisian multipond solar saltern. Extremophiles 2008; 12:505-518.
  • [3] Mutlu MB, Martínez-García M, Santos F, Peña A, Guven K, Antón J. Prokaryotic diversity in Tuz Lake, a hypersaline environment in Inland Turkey. FEMS Microbiol Ecol 2008; 65:474-483.
  • [4] Oh D, Porter K, Russ B, Burns D, Dyall-Smith M. Diversity of Haloquadratum and other haloarchaea in three, geographically distant, Australian saltern crystallizer ponds. Extremophiles 2010; 14:161-169.
  • [5] Ghai R, Pašić L, Fernández AB, Martin-Cuadrado AB, Mizuno CM, McMahon KD, Papke RT, Stepanauskas R, Rodriguez-Brito B, Rohwer F, et al. New abundant microbial groups in aquatic hypersaline environments. Sci Rep 2011; 1:135.
  • [6] Narasingarao P, Podell S, Ugalde JA, Brochier-Armanet C, Emerson JB, Brocks JJ, Heidelberg KB, Banfiel JF, Allen EE. De novo metagenomic assembly reveals abundant novel major lineage of Archaea in hypersaline microbial communities. ISME J 2012; 6:81-93.
  • [7] Grant S, Grant WD, Jones BE, Kato C, Li L. Novel archaeal phylotypes from an East African alkaline saltern. Extremophiles 1999; 3:139-145.
  • [8] Podell S, Ugalde JA, Narasingarao P, Banfield JF, Heidelberg KB, Allen EE. Assembly-driven community genomics of a hypersaline microbial ecosystem. PLoS One 2013; 8:e61692.
  • [9] Zhaxybayeva O, Stepanauskas R, Mohan NR, Papke RT. Cell sorting analysis of geographically separated hypersaline environments. Extremophiles 2013; 17:265-275.
  • [10] Martínez-García M, Santos F, Moreno-Paz M, Parro V, Antón J. Unveiling viral-host interactions within the ‘microbial dark matter’. Nat Commun 2014; 5:1-8.
  • [11] La Cono V, Messina E, Rohde M, Arcadi E, Ciordia S, Crisafi F, Denaro R, Ferrer M, Giuliano L, Golyshin PN, et al. Differential polysaccharide utilization is the basis for a nanohaloarchaeon: haloarchaeon symbiosis. BioRxiv 2019; 794461.
  • [12] Hamm JN, Erdmann S, Eloe-Fadrosh EA, Angeloni A, Zhong L, Brownlee C, Williams TJ, Barton K, Carswell S, Smit MA, et al. Unexpected host dependency of Antarctic Nanohaloarchaeota. Proc Natl Acad Sci USA 2019; 116:14661-14670.
  • [13] Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Huttley GA, Fierer N, Gonzalez-Peña A, Goodrich JK, et al. QIIME allows analysis of high-throughput community sequencing data. Nat Methods 2010; 7:335.
  • [14] Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Lozupone CA, Turnbaugh PJ, Fierer N, Knight R. Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proc Natl Acad Sci USA 2011; 108:4516-4522.
  • [15] Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Huntley J, Fierer N, Owens SM, Betley J, Fraser L, Bauer M, et al. Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. ISME J 2012; 6:1621.
  • [16] Apprill A, McNally S, Parsons R, Weber L. Minor revision to V4 region SSU rRNA 806R gene primer greatly increases detection of SAR11 bacterioplankton. Aquat Microb Ecol 2015; 75:129-137.
  • [17] Parada AE, Needham DM, Fuhrman JA. Every base matters: assessing small subunit rRNA primers for marine microbiomes with mock communities, time series and global field samples. Environ Microbiol 2016; 18:1403-1414.
  • [18] Caporaso JG, Bittinger K, Bushman FD, DeSantis TZ, Andersen GL, Knight R. PyNAST: a flexible tool for aligning sequences to a template alignment. Bioinformatics 2009; 26:266-267.
  • [19] Edgar RC. Search and clustering orders of magnitude faster than BLAST. Bioinformatics 2010; 26:2460-2461.
  • [20] Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, Peplies J, Glöckner FO. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 2012; 41:D590-D596.
  • [21] Chaumeil PA, Mussig AJ, Hugenholtz P, Parks DH. GTDB-Tk: a toolkit to classify genomes with the Genome Taxonomy Database. Bioinformatics 2020; 36:1925-1927.
  • [22] DeLong EF. Archaea in coastal marine environments. Proc Natl Acad Sci USA 1992; 89:5685-5689.
  • [23] Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 2004; 32:1792-1797.
  • [24] Stamatakis A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 2014; 30:1312-1313.
  • [25] Ünal H, Küçükyıldırım-Çelik S. Metabarkodlama yaklaşımıyla Tuz Gölü, Türkiye mikroorganizmalarının belirlenmesi için bir pilot çalışma. Avrupa Bilim ve Teknoloji Dergisi 2020; 19:366-374.
  • [26] Chen S, Liu HC, Zhou J, Xiang H. Haloparvum sedimenti gen. nov., sp. nov., a member of the family Haloferacaceae. Int J Syst Evol Microbiol 2016; 66:2327-2334.
  • [27] Kondo Y, Minegishi H, Echigo A, Shimane Y, Kamekura M, Itoh T, Ohkuma M, Tanaka A, Takahashi-Ando N, Fukushima Y, et al. Haloparvum alkalitolerans sp. nov., alkali-tolerant haloarchaeon isolated from commercial salt. Int J Syst Evol Microbiol 2016; 66:5314-5319.
  • [28] Elevi R, Assa P, Birbir M, Ogan A, Oren A. Characterization of extremely halophilic Archaea isolated from the Ayvalik Saltern, Turkey. World J Microb Biot 2004; 20:719-725.
  • [29] Çınar S, Mutlu MB. Comparative analysis of prokaryotic diversity in solar salterns in eastern Anatolia (Turkey). Extremophiles 2016; 20:589-601.
  • [30] Boutaiba S, Hacene H, Bidle KA, Maupin-Furlow JA. Microbial diversity of the hypersaline Sidi Ameur and Himalatt salt lakes of the Algerian Sahara. J Arid Environ 2011; 75:909-916.
  • [31] Finstad KM, Probst AJ, Thomas BC, Andersen GL, Demergasso C, Echeverría A, Amundson RG, Banfield JF. Microbial community structure and the persistence of cyanobacterial populations in salt crusts of the hyperarid Atacama Desert from genome-resolved metagenomics. Front Microbiol 2017; 8:1435.
  • [32] Pagaling E, Wang H, Venables M, Wallace A, Grant WD, Cowan DA, Jones BE, Ma Y, Ventosa A, Heaphy S. Microbial biogeography of six salt lakes in Inner Mongolia, China, and a salt lake in Argentina. Appl Environ Microbiol 2009; 75:5750-5760.
  • [33] Feng Y, Neri U, Gosselin S, Louyakis AS, Papke RT, Gophna U, Gogarten JP. Reconstructing the evolutionary origins of extreme halophilic Archaeal lineages. BioRxiv 2019.
  • [34] Crits‐Christoph A, Gelsinger DR, Ma B, Wierzchos J, Ravel J, Davila A, Casero MC, DiRuggiero J. Functional interactions of archaea, bacteria and viruses in a hypersaline endolithic community. Environ Microbiol 2016; 18:2064-2077.
  • [35] Cui HL, Yang X, Zhou YG, Liu HC, Zhou PJ, Dyall-Smith ML. Halobellus limi sp. nov. and Halobellus salinus sp. nov., isolated from two marine solar salterns. Int J Syst Evol Microbiol 2012; 62:1307-1313.
  • [36] Han D, Cui HL. Haloplanus litoreus sp. nov. and Haloplanus ruber sp. nov., from a marine solar saltern and an aquaculture farm, respectively. Antonie van Leeuwenhoek 2014; 105:679-685.
  • [37] Vavourakis CD, Ghai R, Rodriguez-Valera F, Sorokin DY, Tringe SG, Hugenholtz P, Muyzer G. Metagenomic insights into the uncultured diversity and physiology of microbes in four hypersaline soda lake brines. Front Microbiol 2016; 7:211.

ASSESSING THE DIVERSITY OF PROKARYOTIC COMMUNITIES AND NANOHALOARCHAEAL LINEAGES IN VARIOUS AQUATIC HYPERSALINE HABITATS (TURKEY) USING HIGH-THROUGHPUT SEQUENCING AND CLONING

Yıl 2021, Cilt: 10 Sayı: 1, 57 - 68, 25.01.2021
https://doi.org/10.18036/estubtdc.777824

Öz

IIn this study, distribution of the prokaryotic groups in Tuz Lake, Ayvalık and Tuzlagözü solar salterns was investigated using 16S rRNA gene targeted approaches. The relative abundance of prokaryotic taxa in the samples was detected by using high-throughput sequencing. Operational taxonomic units (OTUs) associated with Haloquadratum were the most abundant in MiSeq reads. Nanohaloarchaeota-related OTUs were rare (<1%) in Ayvalık and Tuzlagözü solar salterns, and around 5% in Tuz Lake. Other OTUs frequently found and shared in the samples were associated with Halorubrum, Halonotius and Salinibacter genera.

Nanohaloarchaeota lineages, whose phylotypes have been frequently detected in diverse hypersaline environments, were examined in more detail by 16S rRNA gene cloning using group-specific primer. Some of the highly represented nanohaloarchaeal phylotypes in the clone libraries showed low similarity to any sequence in the database, generating two distinct clades. One of the novel lineages was found to be prominent in the clone library constructed from Ayvalık sample. Phylotypes showing 95-97% sequence similarity to Ca. Nanopetramus were also highly represented in Ayvalık. Phylotypes frequent in the clone libraries of Tuz Lake and Tuzlagözü samples were associated with a novel lineage, as well as Ca. Nanosalina and its relatives.

Kaynakça

  • [1] Antón J, Llobet‐Brossa E, Rodríguez‐Valera F, Amann R. Fluorescence in situ hybridization analysis of the prokaryotic community inhabiting crystallizer ponds. Environ Microbiol 1999; 1:517-523.
  • [2] Baati H, Guermazi S, Amdouni R, Gharsallah N, Sghir A, Ammar E. Prokaryotic diversity of a Tunisian multipond solar saltern. Extremophiles 2008; 12:505-518.
  • [3] Mutlu MB, Martínez-García M, Santos F, Peña A, Guven K, Antón J. Prokaryotic diversity in Tuz Lake, a hypersaline environment in Inland Turkey. FEMS Microbiol Ecol 2008; 65:474-483.
  • [4] Oh D, Porter K, Russ B, Burns D, Dyall-Smith M. Diversity of Haloquadratum and other haloarchaea in three, geographically distant, Australian saltern crystallizer ponds. Extremophiles 2010; 14:161-169.
  • [5] Ghai R, Pašić L, Fernández AB, Martin-Cuadrado AB, Mizuno CM, McMahon KD, Papke RT, Stepanauskas R, Rodriguez-Brito B, Rohwer F, et al. New abundant microbial groups in aquatic hypersaline environments. Sci Rep 2011; 1:135.
  • [6] Narasingarao P, Podell S, Ugalde JA, Brochier-Armanet C, Emerson JB, Brocks JJ, Heidelberg KB, Banfiel JF, Allen EE. De novo metagenomic assembly reveals abundant novel major lineage of Archaea in hypersaline microbial communities. ISME J 2012; 6:81-93.
  • [7] Grant S, Grant WD, Jones BE, Kato C, Li L. Novel archaeal phylotypes from an East African alkaline saltern. Extremophiles 1999; 3:139-145.
  • [8] Podell S, Ugalde JA, Narasingarao P, Banfield JF, Heidelberg KB, Allen EE. Assembly-driven community genomics of a hypersaline microbial ecosystem. PLoS One 2013; 8:e61692.
  • [9] Zhaxybayeva O, Stepanauskas R, Mohan NR, Papke RT. Cell sorting analysis of geographically separated hypersaline environments. Extremophiles 2013; 17:265-275.
  • [10] Martínez-García M, Santos F, Moreno-Paz M, Parro V, Antón J. Unveiling viral-host interactions within the ‘microbial dark matter’. Nat Commun 2014; 5:1-8.
  • [11] La Cono V, Messina E, Rohde M, Arcadi E, Ciordia S, Crisafi F, Denaro R, Ferrer M, Giuliano L, Golyshin PN, et al. Differential polysaccharide utilization is the basis for a nanohaloarchaeon: haloarchaeon symbiosis. BioRxiv 2019; 794461.
  • [12] Hamm JN, Erdmann S, Eloe-Fadrosh EA, Angeloni A, Zhong L, Brownlee C, Williams TJ, Barton K, Carswell S, Smit MA, et al. Unexpected host dependency of Antarctic Nanohaloarchaeota. Proc Natl Acad Sci USA 2019; 116:14661-14670.
  • [13] Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Huttley GA, Fierer N, Gonzalez-Peña A, Goodrich JK, et al. QIIME allows analysis of high-throughput community sequencing data. Nat Methods 2010; 7:335.
  • [14] Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Lozupone CA, Turnbaugh PJ, Fierer N, Knight R. Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proc Natl Acad Sci USA 2011; 108:4516-4522.
  • [15] Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Huntley J, Fierer N, Owens SM, Betley J, Fraser L, Bauer M, et al. Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. ISME J 2012; 6:1621.
  • [16] Apprill A, McNally S, Parsons R, Weber L. Minor revision to V4 region SSU rRNA 806R gene primer greatly increases detection of SAR11 bacterioplankton. Aquat Microb Ecol 2015; 75:129-137.
  • [17] Parada AE, Needham DM, Fuhrman JA. Every base matters: assessing small subunit rRNA primers for marine microbiomes with mock communities, time series and global field samples. Environ Microbiol 2016; 18:1403-1414.
  • [18] Caporaso JG, Bittinger K, Bushman FD, DeSantis TZ, Andersen GL, Knight R. PyNAST: a flexible tool for aligning sequences to a template alignment. Bioinformatics 2009; 26:266-267.
  • [19] Edgar RC. Search and clustering orders of magnitude faster than BLAST. Bioinformatics 2010; 26:2460-2461.
  • [20] Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, Peplies J, Glöckner FO. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 2012; 41:D590-D596.
  • [21] Chaumeil PA, Mussig AJ, Hugenholtz P, Parks DH. GTDB-Tk: a toolkit to classify genomes with the Genome Taxonomy Database. Bioinformatics 2020; 36:1925-1927.
  • [22] DeLong EF. Archaea in coastal marine environments. Proc Natl Acad Sci USA 1992; 89:5685-5689.
  • [23] Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 2004; 32:1792-1797.
  • [24] Stamatakis A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 2014; 30:1312-1313.
  • [25] Ünal H, Küçükyıldırım-Çelik S. Metabarkodlama yaklaşımıyla Tuz Gölü, Türkiye mikroorganizmalarının belirlenmesi için bir pilot çalışma. Avrupa Bilim ve Teknoloji Dergisi 2020; 19:366-374.
  • [26] Chen S, Liu HC, Zhou J, Xiang H. Haloparvum sedimenti gen. nov., sp. nov., a member of the family Haloferacaceae. Int J Syst Evol Microbiol 2016; 66:2327-2334.
  • [27] Kondo Y, Minegishi H, Echigo A, Shimane Y, Kamekura M, Itoh T, Ohkuma M, Tanaka A, Takahashi-Ando N, Fukushima Y, et al. Haloparvum alkalitolerans sp. nov., alkali-tolerant haloarchaeon isolated from commercial salt. Int J Syst Evol Microbiol 2016; 66:5314-5319.
  • [28] Elevi R, Assa P, Birbir M, Ogan A, Oren A. Characterization of extremely halophilic Archaea isolated from the Ayvalik Saltern, Turkey. World J Microb Biot 2004; 20:719-725.
  • [29] Çınar S, Mutlu MB. Comparative analysis of prokaryotic diversity in solar salterns in eastern Anatolia (Turkey). Extremophiles 2016; 20:589-601.
  • [30] Boutaiba S, Hacene H, Bidle KA, Maupin-Furlow JA. Microbial diversity of the hypersaline Sidi Ameur and Himalatt salt lakes of the Algerian Sahara. J Arid Environ 2011; 75:909-916.
  • [31] Finstad KM, Probst AJ, Thomas BC, Andersen GL, Demergasso C, Echeverría A, Amundson RG, Banfield JF. Microbial community structure and the persistence of cyanobacterial populations in salt crusts of the hyperarid Atacama Desert from genome-resolved metagenomics. Front Microbiol 2017; 8:1435.
  • [32] Pagaling E, Wang H, Venables M, Wallace A, Grant WD, Cowan DA, Jones BE, Ma Y, Ventosa A, Heaphy S. Microbial biogeography of six salt lakes in Inner Mongolia, China, and a salt lake in Argentina. Appl Environ Microbiol 2009; 75:5750-5760.
  • [33] Feng Y, Neri U, Gosselin S, Louyakis AS, Papke RT, Gophna U, Gogarten JP. Reconstructing the evolutionary origins of extreme halophilic Archaeal lineages. BioRxiv 2019.
  • [34] Crits‐Christoph A, Gelsinger DR, Ma B, Wierzchos J, Ravel J, Davila A, Casero MC, DiRuggiero J. Functional interactions of archaea, bacteria and viruses in a hypersaline endolithic community. Environ Microbiol 2016; 18:2064-2077.
  • [35] Cui HL, Yang X, Zhou YG, Liu HC, Zhou PJ, Dyall-Smith ML. Halobellus limi sp. nov. and Halobellus salinus sp. nov., isolated from two marine solar salterns. Int J Syst Evol Microbiol 2012; 62:1307-1313.
  • [36] Han D, Cui HL. Haloplanus litoreus sp. nov. and Haloplanus ruber sp. nov., from a marine solar saltern and an aquaculture farm, respectively. Antonie van Leeuwenhoek 2014; 105:679-685.
  • [37] Vavourakis CD, Ghai R, Rodriguez-Valera F, Sorokin DY, Tringe SG, Hugenholtz P, Muyzer G. Metagenomic insights into the uncultured diversity and physiology of microbes in four hypersaline soda lake brines. Front Microbiol 2016; 7:211.
Toplam 37 adet kaynakça vardır.

Ayrıntılar

Birincil Dil İngilizce
Konular Yapısal Biyoloji
Bölüm Makaleler
Yazarlar

Seval Çınar 0000-0003-4288-5444

Mehmet Burçin Mutlu 0000-0002-9404-6389

Yayımlanma Tarihi 25 Ocak 2021
Yayımlandığı Sayı Yıl 2021 Cilt: 10 Sayı: 1

Kaynak Göster

APA Çınar, S., & Mutlu, M. B. (2021). ASSESSING THE DIVERSITY OF PROKARYOTIC COMMUNITIES AND NANOHALOARCHAEAL LINEAGES IN VARIOUS AQUATIC HYPERSALINE HABITATS (TURKEY) USING HIGH-THROUGHPUT SEQUENCING AND CLONING. Eskişehir Teknik Üniversitesi Bilim Ve Teknoloji Dergisi - C Yaşam Bilimleri Ve Biyoteknoloji, 10(1), 57-68. https://doi.org/10.18036/estubtdc.777824
AMA Çınar S, Mutlu MB. ASSESSING THE DIVERSITY OF PROKARYOTIC COMMUNITIES AND NANOHALOARCHAEAL LINEAGES IN VARIOUS AQUATIC HYPERSALINE HABITATS (TURKEY) USING HIGH-THROUGHPUT SEQUENCING AND CLONING. Eskişehir Teknik Üniversitesi Bilim ve Teknoloji Dergisi - C Yaşam Bilimleri Ve Biyoteknoloji. Ocak 2021;10(1):57-68. doi:10.18036/estubtdc.777824
Chicago Çınar, Seval, ve Mehmet Burçin Mutlu. “ASSESSING THE DIVERSITY OF PROKARYOTIC COMMUNITIES AND NANOHALOARCHAEAL LINEAGES IN VARIOUS AQUATIC HYPERSALINE HABITATS (TURKEY) USING HIGH-THROUGHPUT SEQUENCING AND CLONING”. Eskişehir Teknik Üniversitesi Bilim Ve Teknoloji Dergisi - C Yaşam Bilimleri Ve Biyoteknoloji 10, sy. 1 (Ocak 2021): 57-68. https://doi.org/10.18036/estubtdc.777824.
EndNote Çınar S, Mutlu MB (01 Ocak 2021) ASSESSING THE DIVERSITY OF PROKARYOTIC COMMUNITIES AND NANOHALOARCHAEAL LINEAGES IN VARIOUS AQUATIC HYPERSALINE HABITATS (TURKEY) USING HIGH-THROUGHPUT SEQUENCING AND CLONING. Eskişehir Teknik Üniversitesi Bilim ve Teknoloji Dergisi - C Yaşam Bilimleri Ve Biyoteknoloji 10 1 57–68.
IEEE S. Çınar ve M. B. Mutlu, “ASSESSING THE DIVERSITY OF PROKARYOTIC COMMUNITIES AND NANOHALOARCHAEAL LINEAGES IN VARIOUS AQUATIC HYPERSALINE HABITATS (TURKEY) USING HIGH-THROUGHPUT SEQUENCING AND CLONING”, Eskişehir Teknik Üniversitesi Bilim ve Teknoloji Dergisi - C Yaşam Bilimleri Ve Biyoteknoloji, c. 10, sy. 1, ss. 57–68, 2021, doi: 10.18036/estubtdc.777824.
ISNAD Çınar, Seval - Mutlu, Mehmet Burçin. “ASSESSING THE DIVERSITY OF PROKARYOTIC COMMUNITIES AND NANOHALOARCHAEAL LINEAGES IN VARIOUS AQUATIC HYPERSALINE HABITATS (TURKEY) USING HIGH-THROUGHPUT SEQUENCING AND CLONING”. Eskişehir Teknik Üniversitesi Bilim ve Teknoloji Dergisi - C Yaşam Bilimleri Ve Biyoteknoloji 10/1 (Ocak 2021), 57-68. https://doi.org/10.18036/estubtdc.777824.
JAMA Çınar S, Mutlu MB. ASSESSING THE DIVERSITY OF PROKARYOTIC COMMUNITIES AND NANOHALOARCHAEAL LINEAGES IN VARIOUS AQUATIC HYPERSALINE HABITATS (TURKEY) USING HIGH-THROUGHPUT SEQUENCING AND CLONING. Eskişehir Teknik Üniversitesi Bilim ve Teknoloji Dergisi - C Yaşam Bilimleri Ve Biyoteknoloji. 2021;10:57–68.
MLA Çınar, Seval ve Mehmet Burçin Mutlu. “ASSESSING THE DIVERSITY OF PROKARYOTIC COMMUNITIES AND NANOHALOARCHAEAL LINEAGES IN VARIOUS AQUATIC HYPERSALINE HABITATS (TURKEY) USING HIGH-THROUGHPUT SEQUENCING AND CLONING”. Eskişehir Teknik Üniversitesi Bilim Ve Teknoloji Dergisi - C Yaşam Bilimleri Ve Biyoteknoloji, c. 10, sy. 1, 2021, ss. 57-68, doi:10.18036/estubtdc.777824.
Vancouver Çınar S, Mutlu MB. ASSESSING THE DIVERSITY OF PROKARYOTIC COMMUNITIES AND NANOHALOARCHAEAL LINEAGES IN VARIOUS AQUATIC HYPERSALINE HABITATS (TURKEY) USING HIGH-THROUGHPUT SEQUENCING AND CLONING. Eskişehir Teknik Üniversitesi Bilim ve Teknoloji Dergisi - C Yaşam Bilimleri Ve Biyoteknoloji. 2021;10(1):57-68.