THE FIRST REPORT OF GEOSMIN AND 2-METHYLISOBORNEOL PRODUCER CYANOBACTERIA FROM TURKISH FRESHWATERS
Year 2021,
Volume: 22 Issue: 2, 163 - 171, 15.10.2021
Zuhal Tunç
,
Reyhan Akçaalan
,
Latife Köker
,
Meriç Albay
Abstract
Water users consider the safety of water according to its aesthetic properties, primarily taste and odour. Geosmin (GEO) and 2-methylisoborneol (MIB) are the most common taste and odour compounds in freshwaters which cause an earthy and musty odour in water. Since human nose can detect these compounds in concentrations as low as 10 ng/L, it is essential to monitor drinking waters before consumer complaints and to produce a timely solution. Therefore, it is necessary to identify GEO and MIB producers to manage the problem at its source. Cyanobacteria are one of the main producers of these compounds in freshwater ecosystems. In this study, we analyzed 13 samples (9 cyanobacteria cultures from Bafa Lake, Elmalı Dam Lake, İznik Lake, Küçükçekmece Lake, Manyas Lake and Taşkısığı Lake, and 4 environmental water samples from Erfelek and Günpınar Waterfalls and Ömerli Dam Lake) for GEO and MIB production by HS-SPME (Head space-solid phase microextraction) coupled with GC-MS (gas chromatography-mass spectrometry). The presence of Cyanobacteria-specific GEO and MIB synthase genes were also analyzed by PCR (Polymerase Chain Reaction). Taste and odour production was confirmed in 2 samples by GC-MS while 4 samples yielded positive results by PCR. All positive samples were environmental samples (3 samples from waterfalls from Günpınar and Erfelek Waterfalls, 1 sample from Ömerli Dam Lake -a drinking water reservoir) which were dominated by Nostoc Vaucher ex Bornet & Flahault, Phormidium Kützing ex Gomont and Pseudanabaena Lauterborn. This is the first report of GEO and MIB producing cyanobacteria in Turkish freshwaters by combining microscopy, analytical and molecular techniques.
Supporting Institution
Research Fund of Istanbul University
Project Number
FYL-2016-20569
Thanks
The authors are grateful to Ayça Oğuz (Istanbul University, Turkey) for microscopy images. We thank Cüneyt Nadir Solak (Dumlupınar University, Turkey) and Fatma Çevik (Çukurova University, Turkey) for waterfall samples. We thank Suvi Suurnäkki & Kaarina Sivonen (Helsinki University, Finland) for their generous gift Oscillatoria sp. UHCC 0332 as a positive control sample for our work. Also, we would like to acknowledge the European Cooperation in Science and Technology, COST Action CA18225 ‘WaterTOP’ for adding value to this study through networking and knowledge sharing with European researchers.
References
- 1. Akcaalan, R., Köker, L., Gürevin, C. & Albay, M. 2014a. Planktothrix rubescens: a perennial presence and toxicity in Lake Sapanca. Turkish Journal of Botany, 38(4): 782-789.
- 2. Akcaalan, R., Köker, L., Oğuz, A., Spoof, L., Meriluoto, J. & Albay, M. 2014b. First report of cylindrospermopsin production by two cyanobacteria (Dolichospermum mendotae and Chrysosporum ovalisporum) in Lake Iznik, Turkey. Toxins (Basel), 6(11): 3173-3186.
- 3. Akcaalan, R., Mazur-Marzec, H., Zalewska, A. & Albay, M. 2009. Phenotypic and toxicological characterization of toxic Nodularia spumigena from a freshwater lake in Turkey. Harmful Algae, 8(2): 273-278.
- 4. Albay, M., Yüksel, Ş., Özel, A.H., Gürevin, C., Oğuz, B. & Akçaalan, R. 2009. Environmental factors affecting geosmin and 2-methylisoborneol production in Sapanca Lake, Türkiye. Phycologia, 48: 2.
- 5. Altschul, S.F., Gish, W., Miller, W., Myers, E. & Lipman, D. 1990. Basic local alignment search tool. Journal of Molecular Biology, 215(3): 403-410.
- 6. Brown, J., Nyfennegger, J., Ang, Y., Simpson, M., MacLeod, B., Wolanin, O. & Gilmore, K. 2020. Biological pretreatment: An innovative approach to addressing taste and odor. AWWA Water Science, 2(2): e1173.
- 7. Cane, D.E., He, X., Kobayashi, S., Omura, S. & Ikeda, H. 2006. Geosmin biosynthesis in Streptomyces avermitilis molecular cloning, expression and mechanistic study of the germacradienol/geosmin synthase. The Journal of Antibiotics (Tokyo), 59(8): 471-479.
- 8. Chong, S., Lee, H. & An, K.G. 2018. Predicting taste and odor compounds in a shallow reservoir using a three–dimensional hydrodynamic ecological model. Water, 10(10): 1396.
- 9. Demir, N., Pulatsu, S., Kirkagac, M.U., Topcu, A., Zencir, O. & Fakıoglu, O. 2011. Phytoplankton composition considering the odor occurrence in the Porsuk River (Eskisehir-Turkey). Asian Journal of Chemistry, 23(1): 247-250.
- 10. Devi, A., Chiu, Y.T., Hsueh, H.T. & Lin, T.F. 2020. Quantitative PCR based detection system for cyanobacterial geosmin/2-methylisoborneol (2-MIB) events in drinking water sources: Current status and challenges. Water Research, 188: 116478.
- 11. Dickschat, J.S., Bode, H.B., Mahmud, T., Müller, R. & Schulz, S. 2005. A novel type of geosmin biosynthesis in myxobacteria. The Journal of Organic Chemistry, 70(13): 5174-5182.
- 12. Fakıoğlu, Ö., Atamanalp, M. & Demir, N. 2011. Toxic blue-green algae in dam lakes. Ankara University Journal of Environmental Sciences, 3(2): 65-71.
- 13. Fakıoğlu, M., Karpuzcu, M.E. & Öztürk, İ. 2018. Evaluation of algae related taste and odor problem in drinking water. Pamukkale University Journal of Engineering Sciences, 24(6): 1141-1156.
- 14. Giglio, S., Jiang, J., Saint, C.P., Cane, D. & Monis, P.T. 2008. Isolation and characterization of the gene associated with geosmin production in cyanobacteria. Environmental Science & Technology, 42(21): 8027-8032.
- 15. Giglio, S., Saint, C.P. & Monis, P.T. 2011. Expression of the geosmin synthase gene in the cyanobacterium Anabaena circinalis AWQC318. Journal of Phycology, 47(6): 1338-1343.
- 16. Godo, T., Saki, Y., Nojiri, Y., Tsujitani, M., Sugahara, S., Hayashi, S., Kamiya, H., Ohtani, S. & Seike, Y. 2017. Geosmin-producing species of Coelosphaerium (Synechococcales, Cyanobacteria) in Lake Shinji, Japan. Scientific Reports, 7(1): 1-10.
- 17. İSKİ (İstanbul Water and Sewerage Administration) 2020. Istanbul Water Quality Reports http://www.iski.gov.tr/ (Date accessed: 10.08.2020).
- 18. Izaguirre, G. & Taylor, W.D. 1998. A Pseudanabaena species from Castaic Lake, California, that produces 2-methylisoborneol. Water Research, 32(5): 1673-1677.
- 19. Izaguirre, G. & Taylor W.D. 2004. A guide to geosmin- and mib-producing cyanobacteria in the United States. Water Science & Technology, 49(9): 19-24.
- 20. Jüttner, F. & Watson, S.B. 2007. Biochemical and ecological control of geosmin and 2-methylisoborneol in source waters. Applied and Environmental Microbiology, 73(14): 4395-4406.
- 21. Kaloudis, T., Triantis, T.M. & Hiskia, A. 2017. Determination of geosmin and 2-methylisoborneol in water by HS-SPME-GC/MS, 469-474. In: Meriluoto, J., Spoof, L & Codd, G.A. (eds). Handbook of Cyanobacterial Monitoring and Cyanotoxin Analysis. John Wiley & Sons, Chichester, 576 pp.
- 22. Koker, L., Akcaalan, R., Oguz, A., Gaygusuz, O., Gurevin, C., Akat Kose, C., Gucver, S., Karaaslan, Y., Erturk, A., Albay, M. & Kinaci, C. 2017. Distribution of toxic cyanobacteria and cyanotoxins in Turkish waterbodies. Journal of Environmental Protection and Ecology, 18(2): 425-432.
- 23. Komárek, J. 2013. Cyanoprokaryota: 3rd Part Heterocytous Genera. Springer-Verlag, Berlin/Heidelberg, 1130 pp.
- 24. Komárek, J. & Anagnostidis, K. 2005. Cyanoprokaryota: 2nd Part Oscillatoriales. Elsevier Spektrum Akademischer Verlag, München, 759 pp.
- 25. Kutovaya, O.A. & Watson, S.B. 2014. Development and application of a molecular assay to detect and monitor geosmin-producing cyanobacteria and actinomycetes in the Great Lakes. Journal of Great Lakes Research, 40(2): 404-414.
- 26. Lee, J., Rai, P.K., Jeon, Y.J., Kim, K.H. & Kwon, E.E. 2017. The role of algae and cyanobacteria in the production and release of odorants in water. Environmental Pollution, 227: 252-262.
- 27. Mattheis, J.P. & Roberts, R.G. 1992. Identification of geosmin as a volatile metabolite of Penicillium expansum. Applied and Environmental Microbiology, 58(9): 3170-3172.
28. Milovanović, I., Mišan, A., Simeunović, J., Kovač, D., Jambrec, D. & Mandić, A. 2015. Determination of volatile organic compounds in selected strains of cyanobacteria. Journal of Chemistry, 2015. http://dx.doi.org/10.1155/2015/969542
- 29. NHMRC, NRMMC 2011. Australian Drinking Water Guidelines. National Water Quality Management Strategy. National Health and Medical Research Council, National Resource Management Ministerial Council, Commonwealth of Australia, Canberra. https://www.nhmrc.gov.au/file/16934/download?token=gAKh3uQk (Date accessed: 12.12.2020).
- 30. Niiyama, Y., Tuji, A., Takemoto, K. & Ichise, S. 2016. Pseudanabaena foetida sp. nov. and P. subfoetida sp. nov. (Cyanophyta/Cyanobacteria) producing 2-methylisoborneol from Japan. Fottea Olomouc, 16(1):1-11.
- 31. Otten, T.G., Graham, J.L., Harris, T.D. & Dreher, T.W. 2016. Elucidation of taste-and odor-producing bacteria and toxigenic cyanobacteria in a midwestern drinking water supply reservoir by shotgun metagenomic analysis. Applied and Environmental Microbiology, 82(17): 5410-5420.
- 32. Pham, T. L., Bui, M.H., Driscoll, M., Shimizu, K., & Motoo, U. 2020. First report of geosmin and 2-methylisoborneol (2-MIB) in Dolichospermum and Oscillatoria from Vietnam. Limnology, 22(1): 43-56.
- 33. Piriou, P., Devesa, R., De Lalande, M. & Glucina, K. 2009. European reassessment of MIB and geosmin perception in drinking water. Journal of Water Supply: Research and Technology—AQUA, 58(8), 532-538.
- 34. Popin, R.V., Rigonato,. J, Abreu, V.A.C., Andreote, A.P.D., Silveira, S.B., Odebrecht, C. & Fiore, M.F. 2016. Draft genome assembly of the bloom-forming cyanobacterium Nodularia spumigena strain CENA596 in shrimp production ponds. Genome Announcements, 4(3): e00466-16.
- 35. Rippka, R., Deruelles, J., Waterbury, J.B., Herdman, M. & Stanier, R.Y. 1979. Generic assignments, strain histories and properties of pure cultures of cyanobacteria. The Journal of General Microbiology, 111(1): 1-61.
- 36. Saker, M.L., Jungblut, A.-D., Neilan, B.A., Rawn, D.F.K. & Vasconcelos, V.M. 2005. Detection of microcystin synthetase genes in health food supplements containing the freshwater cyanobacterium Aphanizomenon flos-aquae. Toxicon, 46(5): 555-562.
- 37. Sugiura, N., Iwami, N. & Inamori, Y. 1998. Significance of attached cyanobacteria relevant to the occurrence of musty odor in Lake Kasumigaura. Water Research, 32(12): 3549-3554.
- 38. Suurnäkki, S., Gomez-Saez, G.V., Rantala-Ylinen, A., Jokela, J., Fewer, D. & Sivonen, K. 2015. Identification of geosmin and 2-methylisoborneol in cyanobacteria and molecular detection methods for the producers of these compounds. Water Research, 68: 56-66.
- 39. Taşkın E., Akbulut A., Yıldız A., Şahin B., Şen B., Uzunöz C., Solak C.N., Başdemir D., Çevik F., Sönmez F., Açikgöz İ., Pabuçcu K., Öztürk M., Alp M.T., Albay M., Çakır M., Özbay Ö., Can Ö., Akçaalan Albay R., Atıcı T., Koray T., Özer T., Karan T., Aktan Turan Y. & Tunç Zengin Z. 2019. A Checklist Of The Flora Of Turkey (Algae). Ali Nihat Gökyiğit Vakfı, İstanbul, 804 pp.
- 40. Tillett, D. & Neilan, B.A. 2000. Xanthogenate nucleic acid ısolation from cultured and environmental cyanobacteria. Journal of Phycology, 36(1): 251-258.
- 41. Wakayama, H. 2003. Revision of Drinking Water Quality Standards in Japan, Ministry of Health Labour and Welfare, Japan. http://www.nilim.go.jp/lab/bcg/siryou/tnn/tnn0264pdf/ks0264011.pdf (Date accessed: 12.12.2020).
- 42. Wang, Z., Xu, Y., Shao, J., Wang, J. & Li, R. 2011. Genes associated with 2-methylisoborneol biosynthesis in cyanobacteria: isolation, characterization, and expression in response to light. PLoS One, 6(4): e18665.
- 43. Wang, Z., Song, G., Shao, J., Tan, W., Li, Y. & Li, R. 2016. Establishment and field applications of real-time PCR methods for the quantification of potential mib-producing cyanobacteria in aquatic systems. Journal of Applied Phycology, 28: 325-333.
- 44. Watson, S.B. 2003. Cyanobacterial and eukaryotic algal odour compounds: signals or by-products? A review of their biological activity. Phycologia, 42(4): 332-350.
- 45. Watson, S.B., Monis, P., Baker, P. & Giglio, S. 2016. Biochemistry and genetics of taste- and odor-producing cyanobacteria. Harmful Algae, 54: 112-127.
- 46. Watson, S.B. & Jüttner, F. 2019. Biological production of taste and odour compounds, taste and odour in source and drinking water: causes, controls, and consequences, 63-112. In: Lin, T.F., Watson, S., Dietrich, A.M. & Suffet, I.H. (eds). Taste and Odour ln Source and Drinking Water: Causes, Controls, and Consequences. IWA Publishing, London, 322 pp.
- 47. Webber, M.A., Atherton, P. & Newcombe, G. 2015. Taste and odour and public perceptions: what do our customers really think about their drinking water? Journal of Water Supply: Research and Technology-Aqua, 64(7): 802-811.
- 48. Zhang, T., Zheng, L., Li, L. & Song, L. 2016. 2-methylisoborneol production characteristics of Pseudanabaena sp. FACHB 1277 isolated from Xionghe Reservoir, China. Journal of Applied Phycology, 28: 3353-3362.
- 49. Zhang, J., Li, L., Qiu, L., Wang, X., Meng, X., You, Y., Yu, J. & Ma, W. 2017. Effects of climate change on 2-methylisoborneol production in two cyanobacterial species. Water, 9(11): 859.
- 50. Zuo, Z. 2019. Why algae release volatile organic compounds-the emission and roles. Frontiers in Microbiology, 10: 491.
Year 2021,
Volume: 22 Issue: 2, 163 - 171, 15.10.2021
Zuhal Tunç
,
Reyhan Akçaalan
,
Latife Köker
,
Meriç Albay
Abstract
Su kullanıcıları, suyun güvenli olup olmadıklarına öncelikle onun tat ve kokusu gibi estetik özelliklerine bakarak karar vermektedir. Geosmin (GEO) ve 2-methylisoborneol (MIB), tatlısularda en yaygın olarak görülen tat ve koku bileşikleridir ve suyun toprak ve küf kokmasına neden olurlar. İnsanlar <10 ng/L gibi düşük konsantrasyonlarda dahi bu kokulara hassas olmalarından dolayı bu bileşiklerin içme sularında tüketici şikayetleri oluşmadan önce izlenmesi ve sorunun çözülmesi oldukça önemlidir. Bu sebeple, problemin kaynağında çözümlenebilmesi için GEO ve MIB üreticilerinin tespit edilmesi gereklidir. Tatlısu ekosistemlerinde bu bileşiklerin başlıca üreticilerinden biri siyanobakterilerdir (Cyanobacteria). Bu çalışmada 13 örnek (9 siyanobakteri kültürü, Bafa Gölü, Elmalı Baraj Gölü, İznik Gölü, Küçükçekmece Gölü, Manyas Gölü, Taşkısığı Gölü’nden ve 4 çevresel su örneği, Günpınar, Erfelek şelaleleri ve Ömerli Baraj Gölü’nden) GEO ve MIB üretiminin tespiti için HS-SPME (Tepe Boşluğu-Katı Faz Mikro Ekstraksiyon) GC-MS (Gaz Kromatografi-Kütle Spektrometresi) yöntemi kullanılarak analiz edilmiştir. Ayrıca siyanobakterilere özgü GEO ve MIB sentaz genlerinin varlığının tespiti için PZR (Polimeraz Zincir Reaksiyonu) yöntemi kullanılmıştır. İki örnekte GC-MS ile tat ve koku üretimi tespit edilmiş ve 4 örnekte de PZR ile pozitif sonuç alınmıştır. Pozitif sonuç elde edilen örnekler Nostoc Vaucher ex Bornet & Flahault, Phormidium Kützing ex Gomont ve Pseudanabaena Lauterborn cinslerinin baskın olduğu çevresel örneklerdir (3 şelale, 1 içme suyu kaynağı örneği). Bu çalışma Türkiye tatlısularındaki tat ve koku üreticisi siyanobakterilerin mikroskobik, analitik ve moleküler yöntemler birlikte kullanılarak tespit edildiği ilk kayıttır.
Project Number
FYL-2016-20569
References
- 1. Akcaalan, R., Köker, L., Gürevin, C. & Albay, M. 2014a. Planktothrix rubescens: a perennial presence and toxicity in Lake Sapanca. Turkish Journal of Botany, 38(4): 782-789.
- 2. Akcaalan, R., Köker, L., Oğuz, A., Spoof, L., Meriluoto, J. & Albay, M. 2014b. First report of cylindrospermopsin production by two cyanobacteria (Dolichospermum mendotae and Chrysosporum ovalisporum) in Lake Iznik, Turkey. Toxins (Basel), 6(11): 3173-3186.
- 3. Akcaalan, R., Mazur-Marzec, H., Zalewska, A. & Albay, M. 2009. Phenotypic and toxicological characterization of toxic Nodularia spumigena from a freshwater lake in Turkey. Harmful Algae, 8(2): 273-278.
- 4. Albay, M., Yüksel, Ş., Özel, A.H., Gürevin, C., Oğuz, B. & Akçaalan, R. 2009. Environmental factors affecting geosmin and 2-methylisoborneol production in Sapanca Lake, Türkiye. Phycologia, 48: 2.
- 5. Altschul, S.F., Gish, W., Miller, W., Myers, E. & Lipman, D. 1990. Basic local alignment search tool. Journal of Molecular Biology, 215(3): 403-410.
- 6. Brown, J., Nyfennegger, J., Ang, Y., Simpson, M., MacLeod, B., Wolanin, O. & Gilmore, K. 2020. Biological pretreatment: An innovative approach to addressing taste and odor. AWWA Water Science, 2(2): e1173.
- 7. Cane, D.E., He, X., Kobayashi, S., Omura, S. & Ikeda, H. 2006. Geosmin biosynthesis in Streptomyces avermitilis molecular cloning, expression and mechanistic study of the germacradienol/geosmin synthase. The Journal of Antibiotics (Tokyo), 59(8): 471-479.
- 8. Chong, S., Lee, H. & An, K.G. 2018. Predicting taste and odor compounds in a shallow reservoir using a three–dimensional hydrodynamic ecological model. Water, 10(10): 1396.
- 9. Demir, N., Pulatsu, S., Kirkagac, M.U., Topcu, A., Zencir, O. & Fakıoglu, O. 2011. Phytoplankton composition considering the odor occurrence in the Porsuk River (Eskisehir-Turkey). Asian Journal of Chemistry, 23(1): 247-250.
- 10. Devi, A., Chiu, Y.T., Hsueh, H.T. & Lin, T.F. 2020. Quantitative PCR based detection system for cyanobacterial geosmin/2-methylisoborneol (2-MIB) events in drinking water sources: Current status and challenges. Water Research, 188: 116478.
- 11. Dickschat, J.S., Bode, H.B., Mahmud, T., Müller, R. & Schulz, S. 2005. A novel type of geosmin biosynthesis in myxobacteria. The Journal of Organic Chemistry, 70(13): 5174-5182.
- 12. Fakıoğlu, Ö., Atamanalp, M. & Demir, N. 2011. Toxic blue-green algae in dam lakes. Ankara University Journal of Environmental Sciences, 3(2): 65-71.
- 13. Fakıoğlu, M., Karpuzcu, M.E. & Öztürk, İ. 2018. Evaluation of algae related taste and odor problem in drinking water. Pamukkale University Journal of Engineering Sciences, 24(6): 1141-1156.
- 14. Giglio, S., Jiang, J., Saint, C.P., Cane, D. & Monis, P.T. 2008. Isolation and characterization of the gene associated with geosmin production in cyanobacteria. Environmental Science & Technology, 42(21): 8027-8032.
- 15. Giglio, S., Saint, C.P. & Monis, P.T. 2011. Expression of the geosmin synthase gene in the cyanobacterium Anabaena circinalis AWQC318. Journal of Phycology, 47(6): 1338-1343.
- 16. Godo, T., Saki, Y., Nojiri, Y., Tsujitani, M., Sugahara, S., Hayashi, S., Kamiya, H., Ohtani, S. & Seike, Y. 2017. Geosmin-producing species of Coelosphaerium (Synechococcales, Cyanobacteria) in Lake Shinji, Japan. Scientific Reports, 7(1): 1-10.
- 17. İSKİ (İstanbul Water and Sewerage Administration) 2020. Istanbul Water Quality Reports http://www.iski.gov.tr/ (Date accessed: 10.08.2020).
- 18. Izaguirre, G. & Taylor, W.D. 1998. A Pseudanabaena species from Castaic Lake, California, that produces 2-methylisoborneol. Water Research, 32(5): 1673-1677.
- 19. Izaguirre, G. & Taylor W.D. 2004. A guide to geosmin- and mib-producing cyanobacteria in the United States. Water Science & Technology, 49(9): 19-24.
- 20. Jüttner, F. & Watson, S.B. 2007. Biochemical and ecological control of geosmin and 2-methylisoborneol in source waters. Applied and Environmental Microbiology, 73(14): 4395-4406.
- 21. Kaloudis, T., Triantis, T.M. & Hiskia, A. 2017. Determination of geosmin and 2-methylisoborneol in water by HS-SPME-GC/MS, 469-474. In: Meriluoto, J., Spoof, L & Codd, G.A. (eds). Handbook of Cyanobacterial Monitoring and Cyanotoxin Analysis. John Wiley & Sons, Chichester, 576 pp.
- 22. Koker, L., Akcaalan, R., Oguz, A., Gaygusuz, O., Gurevin, C., Akat Kose, C., Gucver, S., Karaaslan, Y., Erturk, A., Albay, M. & Kinaci, C. 2017. Distribution of toxic cyanobacteria and cyanotoxins in Turkish waterbodies. Journal of Environmental Protection and Ecology, 18(2): 425-432.
- 23. Komárek, J. 2013. Cyanoprokaryota: 3rd Part Heterocytous Genera. Springer-Verlag, Berlin/Heidelberg, 1130 pp.
- 24. Komárek, J. & Anagnostidis, K. 2005. Cyanoprokaryota: 2nd Part Oscillatoriales. Elsevier Spektrum Akademischer Verlag, München, 759 pp.
- 25. Kutovaya, O.A. & Watson, S.B. 2014. Development and application of a molecular assay to detect and monitor geosmin-producing cyanobacteria and actinomycetes in the Great Lakes. Journal of Great Lakes Research, 40(2): 404-414.
- 26. Lee, J., Rai, P.K., Jeon, Y.J., Kim, K.H. & Kwon, E.E. 2017. The role of algae and cyanobacteria in the production and release of odorants in water. Environmental Pollution, 227: 252-262.
- 27. Mattheis, J.P. & Roberts, R.G. 1992. Identification of geosmin as a volatile metabolite of Penicillium expansum. Applied and Environmental Microbiology, 58(9): 3170-3172.
28. Milovanović, I., Mišan, A., Simeunović, J., Kovač, D., Jambrec, D. & Mandić, A. 2015. Determination of volatile organic compounds in selected strains of cyanobacteria. Journal of Chemistry, 2015. http://dx.doi.org/10.1155/2015/969542
- 29. NHMRC, NRMMC 2011. Australian Drinking Water Guidelines. National Water Quality Management Strategy. National Health and Medical Research Council, National Resource Management Ministerial Council, Commonwealth of Australia, Canberra. https://www.nhmrc.gov.au/file/16934/download?token=gAKh3uQk (Date accessed: 12.12.2020).
- 30. Niiyama, Y., Tuji, A., Takemoto, K. & Ichise, S. 2016. Pseudanabaena foetida sp. nov. and P. subfoetida sp. nov. (Cyanophyta/Cyanobacteria) producing 2-methylisoborneol from Japan. Fottea Olomouc, 16(1):1-11.
- 31. Otten, T.G., Graham, J.L., Harris, T.D. & Dreher, T.W. 2016. Elucidation of taste-and odor-producing bacteria and toxigenic cyanobacteria in a midwestern drinking water supply reservoir by shotgun metagenomic analysis. Applied and Environmental Microbiology, 82(17): 5410-5420.
- 32. Pham, T. L., Bui, M.H., Driscoll, M., Shimizu, K., & Motoo, U. 2020. First report of geosmin and 2-methylisoborneol (2-MIB) in Dolichospermum and Oscillatoria from Vietnam. Limnology, 22(1): 43-56.
- 33. Piriou, P., Devesa, R., De Lalande, M. & Glucina, K. 2009. European reassessment of MIB and geosmin perception in drinking water. Journal of Water Supply: Research and Technology—AQUA, 58(8), 532-538.
- 34. Popin, R.V., Rigonato,. J, Abreu, V.A.C., Andreote, A.P.D., Silveira, S.B., Odebrecht, C. & Fiore, M.F. 2016. Draft genome assembly of the bloom-forming cyanobacterium Nodularia spumigena strain CENA596 in shrimp production ponds. Genome Announcements, 4(3): e00466-16.
- 35. Rippka, R., Deruelles, J., Waterbury, J.B., Herdman, M. & Stanier, R.Y. 1979. Generic assignments, strain histories and properties of pure cultures of cyanobacteria. The Journal of General Microbiology, 111(1): 1-61.
- 36. Saker, M.L., Jungblut, A.-D., Neilan, B.A., Rawn, D.F.K. & Vasconcelos, V.M. 2005. Detection of microcystin synthetase genes in health food supplements containing the freshwater cyanobacterium Aphanizomenon flos-aquae. Toxicon, 46(5): 555-562.
- 37. Sugiura, N., Iwami, N. & Inamori, Y. 1998. Significance of attached cyanobacteria relevant to the occurrence of musty odor in Lake Kasumigaura. Water Research, 32(12): 3549-3554.
- 38. Suurnäkki, S., Gomez-Saez, G.V., Rantala-Ylinen, A., Jokela, J., Fewer, D. & Sivonen, K. 2015. Identification of geosmin and 2-methylisoborneol in cyanobacteria and molecular detection methods for the producers of these compounds. Water Research, 68: 56-66.
- 39. Taşkın E., Akbulut A., Yıldız A., Şahin B., Şen B., Uzunöz C., Solak C.N., Başdemir D., Çevik F., Sönmez F., Açikgöz İ., Pabuçcu K., Öztürk M., Alp M.T., Albay M., Çakır M., Özbay Ö., Can Ö., Akçaalan Albay R., Atıcı T., Koray T., Özer T., Karan T., Aktan Turan Y. & Tunç Zengin Z. 2019. A Checklist Of The Flora Of Turkey (Algae). Ali Nihat Gökyiğit Vakfı, İstanbul, 804 pp.
- 40. Tillett, D. & Neilan, B.A. 2000. Xanthogenate nucleic acid ısolation from cultured and environmental cyanobacteria. Journal of Phycology, 36(1): 251-258.
- 41. Wakayama, H. 2003. Revision of Drinking Water Quality Standards in Japan, Ministry of Health Labour and Welfare, Japan. http://www.nilim.go.jp/lab/bcg/siryou/tnn/tnn0264pdf/ks0264011.pdf (Date accessed: 12.12.2020).
- 42. Wang, Z., Xu, Y., Shao, J., Wang, J. & Li, R. 2011. Genes associated with 2-methylisoborneol biosynthesis in cyanobacteria: isolation, characterization, and expression in response to light. PLoS One, 6(4): e18665.
- 43. Wang, Z., Song, G., Shao, J., Tan, W., Li, Y. & Li, R. 2016. Establishment and field applications of real-time PCR methods for the quantification of potential mib-producing cyanobacteria in aquatic systems. Journal of Applied Phycology, 28: 325-333.
- 44. Watson, S.B. 2003. Cyanobacterial and eukaryotic algal odour compounds: signals or by-products? A review of their biological activity. Phycologia, 42(4): 332-350.
- 45. Watson, S.B., Monis, P., Baker, P. & Giglio, S. 2016. Biochemistry and genetics of taste- and odor-producing cyanobacteria. Harmful Algae, 54: 112-127.
- 46. Watson, S.B. & Jüttner, F. 2019. Biological production of taste and odour compounds, taste and odour in source and drinking water: causes, controls, and consequences, 63-112. In: Lin, T.F., Watson, S., Dietrich, A.M. & Suffet, I.H. (eds). Taste and Odour ln Source and Drinking Water: Causes, Controls, and Consequences. IWA Publishing, London, 322 pp.
- 47. Webber, M.A., Atherton, P. & Newcombe, G. 2015. Taste and odour and public perceptions: what do our customers really think about their drinking water? Journal of Water Supply: Research and Technology-Aqua, 64(7): 802-811.
- 48. Zhang, T., Zheng, L., Li, L. & Song, L. 2016. 2-methylisoborneol production characteristics of Pseudanabaena sp. FACHB 1277 isolated from Xionghe Reservoir, China. Journal of Applied Phycology, 28: 3353-3362.
- 49. Zhang, J., Li, L., Qiu, L., Wang, X., Meng, X., You, Y., Yu, J. & Ma, W. 2017. Effects of climate change on 2-methylisoborneol production in two cyanobacterial species. Water, 9(11): 859.
- 50. Zuo, Z. 2019. Why algae release volatile organic compounds-the emission and roles. Frontiers in Microbiology, 10: 491.