The Effect of Temperature on Growth and Odour Production in Three Cyanobacteria Species

Yıl 2024, Cilt: 39 Sayı: 3, 165 – 171, 01.08.2024

Zuhal Zengin , Reyhan Akçaalan

https://doi.org/10.26650/ASE20241465764

Öz

Taste and odour episodes associated with geosmin and 2-methylisoborneol (MIB) produced by Cyanobacteria are common problems affecting drinking water supplies. However, it is difficult to find the source and species responsible for taste and odour production. The aim of this study was to investigate the effect of temperature, one of the most important environmental factors, on the growth and odour production of Microcoleus sp. MCAS-MC01 and compare the results with those of two other odour-producing cyanobacteria (Oscillatoria sp. UHCC 0332 and Phormidium sp. NIVA-CYA 7) isolated and kept in culture collections from geographically different areas. Microcoleus sp. MCASMC01 is a newly isolated geosmin and MIB producer from Türkiye. After complaints arose from consumers in a nearby city, samples were taken and a cyanobacterium, Microcoleus sp., was isolated from the samples and grown in Z8 medium. Experiments were conducted at 20°C and 25°C for 10 weeks, and the growth and MIB-geosmin concentrations of cultures were monitored weekly. The geosmin concentration reached a maximum 65.73 µg/l and the maximum MIB concentration was 626.65 µg/l in the study. Higher temperature had a significant positive effect on MIB levels in Microcoleus sp. MCAS-MC01 and geosmin levels in Phormidium sp. NIVA-CYA7 (p<0.05). On the other hand, the temperature did not affect the growth of all three strains (p>0.05). The results showed that taste and odour problems are species-specific, and in some species, they are stimulated by an increase in temperature. This study contributes to the understanding of taste and odour problems in relation to temperature.

Anahtar Kelimeler

Cyanobacteria, Geosmin, 2-methylisoborneol, Microcoleus, Oscillatoria, Phormidium

Etik Beyan

Ethics committee approval is not required.

Destekleyen Kurum

This study was funded by the Istanbul University Research Fund (Project numbers: 35783 and 37896)

Proje Numarası

Project numbers: 35783 and 37896

Kaynakça

  • Akcaalan, R., Devesa-Garriga, R., Dietrich, A., Steinhaus, M., Dunkel, A., Mall, V., … & Kaloudis, T. (2022). Water taste and odor (T&O): Challenges, gaps and solutions from a perspective of the WaterTOP network. Chemical Engineering Journal Advances, 12, 100409. https://doi.org/10.1016/j.ceja.2022.100409 google scholar
  • Alghanmi, H. A., Fo’ad, M. A., & Al-Taee, M. M. (2018). Effect of light and temperature on new cyanobacteria producers for geosmin and 2-methylisoborneol. Journal of Applied Phycology, 30(1), 319-328. https://doi.org/10.1007/s10811-017-1233-0 google scholar
  • Cai, F., Yu, G., Zhang, K., Chen, Y., Li, Q., Yang, Y., Xie, J., Wang, Y., & Li, R. (2017). Geosmin production and polyphasic characterization of Oscillatoria limosa Agardh ex Gomont isolated from the open canal of a large drinking water system in Tianjin City, China. Harmful Algae, 69, 28-37. https://doi.Org/10.1016/J.HAL.2017.09.006 google scholar
  • Churro, C., Semedo-Aguiar, A. P., Silva, A. D., Pereira-Leal, J. B., & Leite, R. B. (2020). A novel cyanobacterial geosmin producer, revising Geo A distribution and dispersion patterns in Bacteria. Scientific Reports, 10(1), 8679. https://doi.org/10.1038/s41598-020-64774-y google scholar
  • Devi, A., Chiu, Y. T., Hsueh, H. T., & Lin, T. F. (2021). 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. https://doi. org/10.1016/j.watres.2020.116478 google scholar
  • Ernst, A., Deicher, M., Herman, P. M., & Wollenzien, U. I. (2005). Nitrate and phosphate affect cultivability of cyanobacteria from environments with low nutrient levels. Applied and environmental microbiology, 71(6), 3379-3383. https://doi.org/10.1128/AEM.71.6.3379-3383.2005. google scholar
  • Fujimoto, N., Sudo, R., Sugiura, N., & Inamori, Y (1997). Nutrient-limited growth of Microcystis aeruginosa and Phormidium tenue and competition under various N: P supply ratios and temperatures. Limnology and Oceanography, 42(2), 250-256. https://doi. org/10.4319/lo.1997.42.2.0250 google scholar
  • Gaget, V., Hobson, P., Keulen, A., Newton, K., Monis, P., Humpage, A. R., … & Brookes, J. D. (2020). Toolbox for the sampling and monitoring of benthic cyanobacteria. Water research, 169, 115222. https://doi. org/10.1016/j.watres.2019.115222 google scholar
  • Gaget, V., Almuhtaram, H., Kibuye, F., Hobson, P., Zamyadi, A., Wert, E., & Brookes, J. D. (2022). Benthic cyanobacteria: A utility-centred field study. Harmful Algae, 113, 102185. https://doi.org/10.1016/j. hal.2022.102185 google scholar
  • Izaguirre, G., & Taylor, W. D. (1995). Geosmin and 2-methylisoborneol production in a major aqueduct system. Water science and technology, 31(11), 41-48. https://doi.org/10.1016/0273-1223(95)00454-U google scholar
  • The jamovi project (2022). jamovi. (Version 2.3) [Computer Software] (https://www.jamovi.org) google scholar
  • 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. https://doi.org/10.1128/AEM.02250-06 google scholar
  • Kaloudis, T., Triantis, T. M. , & Hiskia, A. (2016). Determination of Geosmin and 2-Methylisoborneol in Water by HS-SPME-GC/MS. In J. Meriluoto, L. Spoof, & G. A. Codd (Eds.), Handbook of Cyanobacterial Monitoring and Cyanotoxin Analysis (1st ed.). John Wiley & Sons, Ltd. https://doi.org/10.1002/9781119068761 google scholar
  • Kassambara (2023) Pipe-friendly Framework for Basic Statistical Tests in R (https://rpkgs.datanovia.com/rstatix/ ) google scholar
  • Li, Z., Hobson, P., An, W., Burch, M. D., House, J., & Yang, M. (2012). Earthy odor compounds production and loss in three cyanobacterial cultures. Water research, 46(16), 5165-5173. https://doi.org/10.1016/j. watres.2012.06.008 google scholar
  • Mantzouki, E., Lürling, M., Fastner, J., de Senerpont Domis, L., Wilk-Wo£niak, E., Koreiviene, J., … & Warming, T. P. (2018). Temperature effects explain continental scale distribution of cyanobacterial toxins. Toxins, 10(4), 156. https://doi.org/10.3390/toxins10040156 google scholar
  • Niiyama, Y., & Tuji, A. (2019). Microcoleus pseudautumnalis sp. nov. (Cyanobacteria, Oscillatoriales) producing 2-methylisoborneol. Bulletin of the National Museum of Nature and Science, 45, 93-101, https://cir.nii.ac.jp/crid/1523388080253362688 google scholar
  • Oikawa, T., Tsunoda, T., Nakahigashi, H., Shimoriku, M., Kanami, T., & Kimura, S. (2015). Musty odor producing benthic cyanobacteria in the Tama River (Japan) and identification of species by genetic analysis. Journal of Water Supply: Research and Technology—AQUA, 64(7), 839-846. https://doi.org/10.2166/aqua.2015.068 google scholar
  • Ozbayram, E.G., Camur, D., Koker, L., Oguz Cam, A., Akcaalan, R., Albay, M. (2022). The effects of climate change on aquatic ecosystems in relation to human health. Aquatic Sciences and Engineering, 37(3), 123-128. https://doi.org/10.26650/ASE20221057160 google scholar
  • Qiu, P., Zhang, Y., Mi, W., Song, G., & Bi, Y. (2023). Producers and drivers of odor compounds in a large drinking-water source. Frontiers in Ecology and Evolution, 11, 1216567. https://doi.org/10.3389/fevo.2023.1216567 google scholar
  • R Core Team (2024) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria (https://www.R-project.org ) google scholar
  • Robarts, R. D., & Zohary, T. (1987). Temperature effects on photosynthetic capacity, respiration, and growth rates of bloom-forming cyanobacteria. New Zealand journal of marine and freshwater research, 21(3), 391-399. https://doi.org/10.1080/00288330.1987.9516235 google scholar
  • Robin, J., Cravedi, J. P., Hillenweck, A., Deshayes, C., & Vallod, D. (2006). Off flavor characterization and origin in French trout farming. Aquaculture, 260(1-4), 128-138. https://doi.org/10.1016/j. aquaculture.2006.05.058 google scholar
  • Shen, Q., Wang, Q., Miao, H., Shimada, M., Utsumi, M., Lei, Z., … & Shimizu, K. (2022). Temperature affects growth, geosmin/2-methylisoborneol production, and gene expression in two cyanobacterial species. Environmental Science and Pollution Research, 29, 12017-12026. https://doi.org/10.1007/s11356-021-16593-5 google scholar
  • Shen, Q., Shimizu, K., Miao, H., Tsukino, S., Utsumi, M., Lei, Z., … & Akiba, M. (2021). Effects of elevated nitrogen on the growth and geosmin productivity of Dolichospermum smithii. Environmental Science and Pollution Research, 28, 177-184. https://doi.org/10.1007/s11356-020-10429-4 google scholar
  • Sivonen, K. (1990). Effects of light, temperature, nitrate, orthophosphate, and bacteria on growth of and hepatotoxin production by Oscillatoria agardhii strains. Applied and environmental microbiology, 56(9), 2658. https://doi.org/10.1128/aem.56.9.2658-2666.1990 google scholar
  • Strunecky, O., Komarek, J., Johansen, J., Lukesova, A., & Elster, J. (2013). Molecular and morphological criteria for revision of the genus Microcoleus (Oscillatoriales, C yanobacteria). Journal of phycology, 49(6), 1167-1180. https://doi.org/10.1111/jpy.12128 google scholar
  • Tee, H. S., Wood, S. A., Bouma-Gregson, K., Lear, G., & Handley, K. M. (2021). Genome streamlining, plasticity, and metabolic versatility distinguish co-occurring toxic and nontoxic cyanobacterial strains of Microcoleus. Mbio, 12(5), e02235-21 https://doi.org/10.1128/mbio.02235-21 google scholar
  • Teneva, I., Belkinova, D., Paunova-Krasteva, T., Bardarov, K., Moten, D., Mladenov, R., & Dzhambazov, B. (2023). Polyphasic characterisation of Microcoleus autumnalis (Gomont, 1892) Strunecky, Komarek & JR Johansen, 2013 (Oscillatoriales, Cyanobacteria) using a metabolomic approach as a complementary tool. Biodiversity Data Journal, 11. https://doi.org/10.3897/BDJ.11.e100525 google scholar
  • Wang, Z., & Li, R. (2015). Effects of light and temperature on the odor production of 2-methylisoborneol-producing Pseudanabaena sp. and geosmin-producing Anabaena ucrainica (cyanobacteria). Biochemical Systematics and Ecology, 58, 219-226. https://doi. org/10.1016/j.bse.2014.12.013 google scholar
  • Watson, S., & Jüttner, F. (2019). Biological production of taste and odour compounds. Taste and Odour in Source and Drinking Water: Causes, Controls, and Consequences. London, UK, IWApublishing, 63-112. https://doi.org/10.2166/9781780406664_0063 google scholar
  • Watson, S. B., Monis, P., Baker, P., & Giglio, S. (2016). Biochemistry and genetics of taste-and odor-producing cyanobacteria. Harmful Algae, 54, 112-127. https://doi.org/10.1016/j.hal.2015.11.008 google scholar
  • Watson, S. B. (2004). Aquatic taste and odor: a primary signal of drinking-water integrity. Journal of Toxicology and Environmental Health, 67(20-22), 1779-1795. https://doi.org/10.1080/15287390490492377 google scholar
  • Zamyadi, A., Henderson, R., Stuetz, R., Hofmann, R., Ho, L., & Newcombe, G. (2015). Fate of geosmin and 2-methylisoborneol in full-scale water treatment plants. Water research, 83, 171-183. https://doi. org/10.1016/j.watres.2015.06.038 google scholar

Yıl 2024, Cilt: 39 Sayı: 3, 165 – 171, 01.08.2024

Zuhal Zengin , Reyhan Akçaalan

https://doi.org/10.26650/ASE20241465764

Öz

Proje Numarası

Project numbers: 35783 and 37896

Kaynakça

  • Akcaalan, R., Devesa-Garriga, R., Dietrich, A., Steinhaus, M., Dunkel, A., Mall, V., … & Kaloudis, T. (2022). Water taste and odor (T&O): Challenges, gaps and solutions from a perspective of the WaterTOP network. Chemical Engineering Journal Advances, 12, 100409. https://doi.org/10.1016/j.ceja.2022.100409 google scholar
  • Alghanmi, H. A., Fo’ad, M. A., & Al-Taee, M. M. (2018). Effect of light and temperature on new cyanobacteria producers for geosmin and 2-methylisoborneol. Journal of Applied Phycology, 30(1), 319-328. https://doi.org/10.1007/s10811-017-1233-0 google scholar
  • Cai, F., Yu, G., Zhang, K., Chen, Y., Li, Q., Yang, Y., Xie, J., Wang, Y., & Li, R. (2017). Geosmin production and polyphasic characterization of Oscillatoria limosa Agardh ex Gomont isolated from the open canal of a large drinking water system in Tianjin City, China. Harmful Algae, 69, 28-37. https://doi.Org/10.1016/J.HAL.2017.09.006 google scholar
  • Churro, C., Semedo-Aguiar, A. P., Silva, A. D., Pereira-Leal, J. B., & Leite, R. B. (2020). A novel cyanobacterial geosmin producer, revising Geo A distribution and dispersion patterns in Bacteria. Scientific Reports, 10(1), 8679. https://doi.org/10.1038/s41598-020-64774-y google scholar
  • Devi, A., Chiu, Y. T., Hsueh, H. T., & Lin, T. F. (2021). 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. https://doi. org/10.1016/j.watres.2020.116478 google scholar
  • Ernst, A., Deicher, M., Herman, P. M., & Wollenzien, U. I. (2005). Nitrate and phosphate affect cultivability of cyanobacteria from environments with low nutrient levels. Applied and environmental microbiology, 71(6), 3379-3383. https://doi.org/10.1128/AEM.71.6.3379-3383.2005. google scholar
  • Fujimoto, N., Sudo, R., Sugiura, N., & Inamori, Y (1997). Nutrient-limited growth of Microcystis aeruginosa and Phormidium tenue and competition under various N: P supply ratios and temperatures. Limnology and Oceanography, 42(2), 250-256. https://doi. org/10.4319/lo.1997.42.2.0250 google scholar
  • Gaget, V., Hobson, P., Keulen, A., Newton, K., Monis, P., Humpage, A. R., … & Brookes, J. D. (2020). Toolbox for the sampling and monitoring of benthic cyanobacteria. Water research, 169, 115222. https://doi. org/10.1016/j.watres.2019.115222 google scholar
  • Gaget, V., Almuhtaram, H., Kibuye, F., Hobson, P., Zamyadi, A., Wert, E., & Brookes, J. D. (2022). Benthic cyanobacteria: A utility-centred field study. Harmful Algae, 113, 102185. https://doi.org/10.1016/j. hal.2022.102185 google scholar
  • Izaguirre, G., & Taylor, W. D. (1995). Geosmin and 2-methylisoborneol production in a major aqueduct system. Water science and technology, 31(11), 41-48. https://doi.org/10.1016/0273-1223(95)00454-U google scholar
  • The jamovi project (2022). jamovi. (Version 2.3) [Computer Software] (https://www.jamovi.org) google scholar
  • 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. https://doi.org/10.1128/AEM.02250-06 google scholar
  • Kaloudis, T., Triantis, T. M. , & Hiskia, A. (2016). Determination of Geosmin and 2-Methylisoborneol in Water by HS-SPME-GC/MS. In J. Meriluoto, L. Spoof, & G. A. Codd (Eds.), Handbook of Cyanobacterial Monitoring and Cyanotoxin Analysis (1st ed.). John Wiley & Sons, Ltd. https://doi.org/10.1002/9781119068761 google scholar
  • Kassambara (2023) Pipe-friendly Framework for Basic Statistical Tests in R (https://rpkgs.datanovia.com/rstatix/ ) google scholar
  • Li, Z., Hobson, P., An, W., Burch, M. D., House, J., & Yang, M. (2012). Earthy odor compounds production and loss in three cyanobacterial cultures. Water research, 46(16), 5165-5173. https://doi.org/10.1016/j. watres.2012.06.008 google scholar
  • Mantzouki, E., Lürling, M., Fastner, J., de Senerpont Domis, L., Wilk-Wo£niak, E., Koreiviene, J., … & Warming, T. P. (2018). Temperature effects explain continental scale distribution of cyanobacterial toxins. Toxins, 10(4), 156. https://doi.org/10.3390/toxins10040156 google scholar
  • Niiyama, Y., & Tuji, A. (2019). Microcoleus pseudautumnalis sp. nov. (Cyanobacteria, Oscillatoriales) producing 2-methylisoborneol. Bulletin of the National Museum of Nature and Science, 45, 93-101, https://cir.nii.ac.jp/crid/1523388080253362688 google scholar
  • Oikawa, T., Tsunoda, T., Nakahigashi, H., Shimoriku, M., Kanami, T., & Kimura, S. (2015). Musty odor producing benthic cyanobacteria in the Tama River (Japan) and identification of species by genetic analysis. Journal of Water Supply: Research and Technology—AQUA, 64(7), 839-846. https://doi.org/10.2166/aqua.2015.068 google scholar
  • Ozbayram, E.G., Camur, D., Koker, L., Oguz Cam, A., Akcaalan, R., Albay, M. (2022). The effects of climate change on aquatic ecosystems in relation to human health. Aquatic Sciences and Engineering, 37(3), 123-128. https://doi.org/10.26650/ASE20221057160 google scholar
  • Qiu, P., Zhang, Y., Mi, W., Song, G., & Bi, Y. (2023). Producers and drivers of odor compounds in a large drinking-water source. Frontiers in Ecology and Evolution, 11, 1216567. https://doi.org/10.3389/fevo.2023.1216567 google scholar
  • R Core Team (2024) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria (https://www.R-project.org ) google scholar
  • Robarts, R. D., & Zohary, T. (1987). Temperature effects on photosynthetic capacity, respiration, and growth rates of bloom-forming cyanobacteria. New Zealand journal of marine and freshwater research, 21(3), 391-399. https://doi.org/10.1080/00288330.1987.9516235 google scholar
  • Robin, J., Cravedi, J. P., Hillenweck, A., Deshayes, C., & Vallod, D. (2006). Off flavor characterization and origin in French trout farming. Aquaculture, 260(1-4), 128-138. https://doi.org/10.1016/j. aquaculture.2006.05.058 google scholar
  • Shen, Q., Wang, Q., Miao, H., Shimada, M., Utsumi, M., Lei, Z., … & Shimizu, K. (2022). Temperature affects growth, geosmin/2-methylisoborneol production, and gene expression in two cyanobacterial species. Environmental Science and Pollution Research, 29, 12017-12026. https://doi.org/10.1007/s11356-021-16593-5 google scholar
  • Shen, Q., Shimizu, K., Miao, H., Tsukino, S., Utsumi, M., Lei, Z., … & Akiba, M. (2021). Effects of elevated nitrogen on the growth and geosmin productivity of Dolichospermum smithii. Environmental Science and Pollution Research, 28, 177-184. https://doi.org/10.1007/s11356-020-10429-4 google scholar
  • Sivonen, K. (1990). Effects of light, temperature, nitrate, orthophosphate, and bacteria on growth of and hepatotoxin production by Oscillatoria agardhii strains. Applied and environmental microbiology, 56(9), 2658. https://doi.org/10.1128/aem.56.9.2658-2666.1990 google scholar
  • Strunecky, O., Komarek, J., Johansen, J., Lukesova, A., & Elster, J. (2013). Molecular and morphological criteria for revision of the genus Microcoleus (Oscillatoriales, C yanobacteria). Journal of phycology, 49(6), 1167-1180. https://doi.org/10.1111/jpy.12128 google scholar
  • Tee, H. S., Wood, S. A., Bouma-Gregson, K., Lear, G., & Handley, K. M. (2021). Genome streamlining, plasticity, and metabolic versatility distinguish co-occurring toxic and nontoxic cyanobacterial strains of Microcoleus. Mbio, 12(5), e02235-21 https://doi.org/10.1128/mbio.02235-21 google scholar
  • Teneva, I., Belkinova, D., Paunova-Krasteva, T., Bardarov, K., Moten, D., Mladenov, R., & Dzhambazov, B. (2023). Polyphasic characterisation of Microcoleus autumnalis (Gomont, 1892) Strunecky, Komarek & JR Johansen, 2013 (Oscillatoriales, Cyanobacteria) using a metabolomic approach as a complementary tool. Biodiversity Data Journal, 11. https://doi.org/10.3897/BDJ.11.e100525 google scholar
  • Wang, Z., & Li, R. (2015). Effects of light and temperature on the odor production of 2-methylisoborneol-producing Pseudanabaena sp. and geosmin-producing Anabaena ucrainica (cyanobacteria). Biochemical Systematics and Ecology, 58, 219-226. https://doi. org/10.1016/j.bse.2014.12.013 google scholar
  • Watson, S., & Jüttner, F. (2019). Biological production of taste and odour compounds. Taste and Odour in Source and Drinking Water: Causes, Controls, and Consequences. London, UK, IWApublishing, 63-112. https://doi.org/10.2166/9781780406664_0063 google scholar
  • Watson, S. B., Monis, P., Baker, P., & Giglio, S. (2016). Biochemistry and genetics of taste-and odor-producing cyanobacteria. Harmful Algae, 54, 112-127. https://doi.org/10.1016/j.hal.2015.11.008 google scholar
  • Watson, S. B. (2004). Aquatic taste and odor: a primary signal of drinking-water integrity. Journal of Toxicology and Environmental Health, 67(20-22), 1779-1795. https://doi.org/10.1080/15287390490492377 google scholar
  • Zamyadi, A., Henderson, R., Stuetz, R., Hofmann, R., Ho, L., & Newcombe, G. (2015). Fate of geosmin and 2-methylisoborneol in full-scale water treatment plants. Water research, 83, 171-183. https://doi. org/10.1016/j.watres.2015.06.038 google scholar

Toplam 34 adet kaynakça vardır.

Ayrıntılar

Birincil Dil İngilizce
Konular Hidrobiyoloji
BölümAraştırma Makalesi
Yazarlar

Zuhal Zengin lstanbul University, Faculty of Aquatic Sciences, Department of Marine and Freshwater Resources Management 0000-0002-6560-6789 Türkiye

Reyhan Akçaalan lstanbul University, Faculty of Aquatic Sciences, Department of Marine and Freshwater Resources Management 0000-0002-0756-8972 Türkiye

Proje NumarasıProject numbers: 35783 and 37896
Yayımlanma Tarihi1 Ağustos 2024
Gönderilme Tarihi5 Nisan 2024
Kabul Tarihi6 Mayıs 2024
Yayımlandığı Sayı Yıl 2024 Cilt: 39 Sayı: 3

Kaynak Göster

APAZengin, Z., & Akçaalan, R. (2024). The Effect of Temperature on Growth and Odour Production in Three Cyanobacteria Species. Aquatic Sciences and Engineering, 39(3), 165-171. https://doi.org/10.26650/ASE20241465764
AMAZengin Z, Akçaalan R. The Effect of Temperature on Growth and Odour Production in Three Cyanobacteria Species. Aqua Sci Eng. Ağustos 2024;39(3):165-171. doi:10.26650/ASE20241465764
ChicagoZengin, Zuhal, ve Reyhan Akçaalan. “The Effect of Temperature on Growth and Odour Production in Three Cyanobacteria Species”. Aquatic Sciences and Engineering 39, sy. 3 (Ağustos 2024): 165-71. https://doi.org/10.26650/ASE20241465764.
EndNoteZengin Z, Akçaalan R (01 Ağustos 2024) The Effect of Temperature on Growth and Odour Production in Three Cyanobacteria Species. Aquatic Sciences and Engineering 39 3 165–171.
IEEEZ. Zengin ve R. Akçaalan, “The Effect of Temperature on Growth and Odour Production in Three Cyanobacteria Species”, Aqua Sci Eng, c. 39, sy. 3, ss. 165–171, 2024, doi: 10.26650/ASE20241465764.
ISNADZengin, Zuhal – Akçaalan, Reyhan. “The Effect of Temperature on Growth and Odour Production in Three Cyanobacteria Species”. Aquatic Sciences and Engineering 39/3 (Ağustos 2024), 165-171. https://doi.org/10.26650/ASE20241465764.
JAMAZengin Z, Akçaalan R. The Effect of Temperature on Growth and Odour Production in Three Cyanobacteria Species. Aqua Sci Eng. 2024;39:165–171.
MLAZengin, Zuhal ve Reyhan Akçaalan. “The Effect of Temperature on Growth and Odour Production in Three Cyanobacteria Species”. Aquatic Sciences and Engineering, c. 39, sy. 3, 2024, ss. 165-71, doi:10.26650/ASE20241465764.
VancouverZengin Z, Akçaalan R. The Effect of Temperature on Growth and Odour Production in Three Cyanobacteria Species. Aqua Sci Eng. 2024;39(3):165-71.

Download or read online: Click here