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Phylogenetic Analysis and Characterization of Odorous Compound-Producing Actinomycetes in Sediments in the Sanbe Reservoir, A Drinking Water Reservoir in Japan

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Abstract

Odor caused by the presence of geosmin and 2-methylisoborneol (2-MIB) in aquatic ecosystems leads to considerable economic loss worldwide. The odorous compounds are primarily produced by cyanobacteria and actinomycetes. While the contribution of odorous compounds-producing cyanobacteria has been thoroughly investigated, the production of geosmin and 2-MIB by actinomycetes in aquatic ecosystems is poorly understood. In this study, we isolated geosmin and/or 2-MIB-producing actinomycetes in sediments collected from the Sanbe Reservoir, Japan, identified the biosynthetic gene of geosmin and 2-MIB, and investigated the production of the odorous compounds by the isolated strains. Partial sequence of 16S rRNA and the biosynthetic genes was determined to analyze the phylogenetic relationship among the strains. The geosmin and 2-MIB concentrations in the culture of the isolated strains were measured using gas chromatography mass spectrometry. Fifty-four strains of odorous compounds-producing and non-geosmin-producing actinomycetes were isolated from sediments from the Sanbe Reservoir. Diverse actinomycetes were identified and many of them produced geosmin and/or 2-MIB. Many odorous compounds-producing actinomycetes were phylogenetically different from previously reported producing actinomycetes. The producing ability of the odorous compounds of the isolated strains in this study was not significantly related with the phylogenetic groups of 16S rRNA and the biosynthetic genes. The findings suggest that the odorous compounds-producing actinomycetes in the sediments are diverse and different from previously reported strains.

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References

  1. Gerber NN, Lecheval HA (1965) Geosmin an Earthy-Smelling Substance Isolated from Actinomycetes. Appl Microbiol 13(6):935–938. https://doi.org/10.1128/Aem.13.6.935-938.1965

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  2. Medsker LL, Jenkins D, Thomas JF, Koch C (1969) Odorous compounds in natural waters. 2-Exo-hydroxy-2-methylbornane major odorous compound produced by several actinomycetes. Environ Sci Technol 3(5):476–477. https://doi.org/10.1021/es60028a008

    Article  CAS  Google Scholar 

  3. Robin J, Cravedi JP, 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

    Article  CAS  Google Scholar 

  4. Devi A, Chiu YT, Hsueh HT, Lin TF (2021) Quantitative PCR based detection system for cyanobacterial geosmin/2-methylisoborneol (2-MIB) events in drinking water sources: current status and challenges. Water Res 188:116478. https://doi.org/10.1016/j.watres.2020.116478

    Article  PubMed  CAS  Google Scholar 

  5. Watson SB, 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

    Article  PubMed  CAS  Google Scholar 

  6. Liato V, Aider M (2017) Geosmin as a source of the earthy-musty smell in fruits, vegetables and water: origins, impact on foods and water, and review of the removing techniques. Chemosphere 181:9–18. https://doi.org/10.1016/j.chemosphere.2017.04.039

    Article  PubMed  CAS  Google Scholar 

  7. Zaitlin B, Watson SB (2006) Actinomycetes in relation to taste and odour in drinking water: myths, tenets and truths. Water Res 40(9):1741–1753. https://doi.org/10.1016/j.watres.2006.02.024

    Article  PubMed  CAS  Google Scholar 

  8. Jüttner F, Watson SB (2007) Biochemical and ecological control of geosmin and 2-methylisoborneol in source waters. Appl Environ Microbiol 73(14):4395–4406. https://doi.org/10.1128/AEM.02250-06

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  9. Callejon RM, Ubeda C, Rios-Reina R, Morales ML, Troncoso AM (2016) Recent developments in the analysis of musty odour compounds in water and wine: a review. J Chromatogr A 1428:72–85. https://doi.org/10.1016/j.chroma.2015.09.008

    Article  PubMed  CAS  Google Scholar 

  10. Sugiura N, Nakano K (2000) Causative microorganisms for musty odor occurrence in the eutrophic Lake Kasumigaura. Hydrobiologia 434(1–3):145–150. https://doi.org/10.1023/A:1004000511610

    Article  CAS  Google Scholar 

  11. Kikuchi T, Kadota S, Suehara H, Nishi A, Tsubaki K, Yano H, Harimaya K (1983) Odorous metabolites of fungi, Chaetomium globosum KINZE ex FR. and Botrytis cinerea PERS. ex FR., and a blue-green alga, Phormidium tenue (MENEGHINI) GOMONT. Chem Pharm Bull (Tokyo) 31(2):659–663

    Article  CAS  Google Scholar 

  12. Trowitzsch W, Witte L, Reichenbach H (1981) Geosmin from earthy smelling cultures of Nannocystis exedens (Myxobacterales). FEMS Microbiol Lett 12(3):257–260

    Article  CAS  Google Scholar 

  13. Anuar NSS, Kassim AA, Utsumi M, Iwamoto K, Goto M, Shimizu K, Othman N, Zakaria Z, Sugiura N, Hara H (2017) Characterization of musty odor-producing actinomycetes from tropics and effects of temperature on the production of musty odor compounds. Microbes Environ 32(4):352–357. https://doi.org/10.1264/jsme2.ME17109

    Article  PubMed  PubMed Central  Google Scholar 

  14. Asquith E, Evans C, Dunstan RH, Geary P, Cole B (2018) Distribution, abundance and activity of geosmin and 2-methylisoborneol-producing Streptomyces in drinking water reservoirs. Water Res 145:30–38. https://doi.org/10.1016/j.watres.2018.08.014

    Article  PubMed  CAS  Google Scholar 

  15. Klausen C, Nicolaisen MH, Strobel BW, Warnecke F, Nielsen JL, Jorgensen NO (2005) Abundance of actinobacteria and production of geosmin and 2-methylisoborneol in Danish streams and fish ponds. FEMS Microbiol Ecol 52(2):265–278. https://doi.org/10.1016/j.femsec.2004.11.015

    Article  PubMed  CAS  Google Scholar 

  16. Zuo Y, Li L, Zhang T, Zheng L, Dai G, Liu L, Song L (2010) Contribution of Streptomyces in sediment to earthy odor in the overlying water in Xionghe Reservoir, China. Water Res 44(20):6085–6094. https://doi.org/10.1016/j.watres.2010.08.001

    Article  PubMed  CAS  Google Scholar 

  17. Tung SC, Lin TF, Tseng IC, Lin HM (2006) Identification of 2-MIB and geosmin producers in Feng-Shen reservoir in south Taiwan. Water Sci Technol-Water Supply 6(2):55–61. https://doi.org/10.2166/ws.2006.050

    Article  CAS  Google Scholar 

  18. Zuo YX, Li L, Wu ZX, Song LR (2009) Isolation, identification and odour-producing abilities of geosmin/2-MIB in actinomycetes from sediments in Lake Lotus, China. J Water Supply Res Technol 58(8):552–561. https://doi.org/10.2166/aqua.2009.018

    Article  CAS  Google Scholar 

  19. Park TJ, Yu MN, Kim HS, Cho HS, Hwang MY, Yang HJ, Lee JC, Lee JK, Kim SJ (2016) Characteristics of actinomycetes producing geosmin in Paldang Lake, Korea. Desalin Water Treat 57(2):888–899. https://doi.org/10.1080/19443994.2014.970583

    Article  CAS  Google Scholar 

  20. 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. Sci Rep 7:41928. https://doi.org/10.1038/srep41928

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  21. Kim K, Park C, Yoon Y, Hwang SJ (2018) Harmful cyanobacterial material production in the North Han River (South Korea): genetic potential and temperature-dependent properties. Int J Env Res Public Health 15(3):444. https://doi.org/10.3390/ijerph15030444

    Article  CAS  Google Scholar 

  22. Churro C, Semedo-Aguiar AP, Silva AD, Pereira-Leal JB, Leite RB (2020) A novel cyanobacterial geosmin producer, revising GeoA distribution and dispersion patterns in Bacteria. Sci Rep 10(1):8679. https://doi.org/10.1038/s41598-020-64774-y

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  23. Hayashi S, Ohtani S, Godo T, Nojiri Y, Saki Y, Esumi T, Kamiya H (2019) Identification of geosmin biosynthetic gene in geosmin-producing colonial cyanobacteria Coelosphaerium sp. and isolation of geosmin non-producing Coelosphaerium sp. from brackish Lake Shinji in Japan. Harmful Algae 84:19–26. https://doi.org/10.1016/j.hal.2019.01.010

    Article  PubMed  CAS  Google Scholar 

  24. Kutovaya OA, Watson SB (2014) Development and application of a molecular assay to detect and monitor geosmin-producing cyanobacteria and actinomycetes in the Great Lakes. J Great Lakes Res 40(2):404–414. https://doi.org/10.1016/j.jglr.2014.03.016

    Article  CAS  Google Scholar 

  25. Jorgensen NOG, Podduturi R, Burford MA (2016) Relations between abundance of potential geosmin- and 2-MIB-producing organisms and concentrations of these compounds in water from three Australian reservoirs. J Water Supply Res Technol 65(6):504–513. https://doi.org/10.2166/aqua.2016.001

    Article  Google Scholar 

  26. Kim S, Hayashi S, Masuki S, Ayukawa K, Ohtani S, Seike Y (2021) Effect of rainfall and pH on musty odor produced in the Sanbe reservoir. Water 13(24):3600. https://doi.org/10.3390/w13243600

    Article  CAS  Google Scholar 

  27. Sugihara K, Takada K, Yamashita S (2005) Modeling of musty odor caused by actinomycetes in dam reservoir. Mon. Rep Civ Eng Res Inst 630:10–22 (in Japanese)

    Google Scholar 

  28. Otoguro M, Nakashima T, Miyadoh S (2012) Isolation of actinomycetes and search of antibiotics. Seibutsu-kogaku kaishi 90(8):493–498 (in Japanese)

    CAS  Google Scholar 

  29. Weisburg WG, Barns SM, Pelletier DA, Lane DJ (1991) 16S ribosomal DNA amplification for phylogenetic study. J Bacteriol 173(2):697–703

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  30. Huong NL, Itoh K, Suyama K (2007) Diversity of 2,4-dichlorophenoxyacetic acid (2,4-D) and 2,4,5-trichlorophenoxyacetic acid (2,4,5-T)-degrading bacteria in Vietnamese soils. Microbes Environ 22(3):243–256. https://doi.org/10.1264/jsme2.22.243

    Article  Google Scholar 

  31. Du H, Lu H, Xu Y, Du X (2013) Community of environmental streptomyces related to geosmin development in Chinese liquors. J Agric Food Chem 61(6):1343–1348. https://doi.org/10.1021/jf3040513

    Article  PubMed  CAS  Google Scholar 

  32. Kumar S, Stecher G, Tamura K (2016) MEGA7: Molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  33. Cane DE, Ikeda H (2012) Exploration and mining of the bacterial terpenome. Acc Chem Res 45(3):463–472. https://doi.org/10.1021/ar200198d

    Article  PubMed  CAS  Google Scholar 

  34. Auffret M, Pilote A, Proulx E, Proulx D, Vandenberg G, Villemur R (2011) Establishment of a real-time PCR method for quantification of geosmin-producing Streptomyces spp. in recirculating aquaculture systems. Water Res 45(20):6753–6762. https://doi.org/10.1016/j.watres.2011.10.020

    Article  PubMed  CAS  Google Scholar 

  35. Schrader KK, Summerfelt ST (2010) Distribution of off-favor compounds and isolation of geosmin-producing bacteria in a series of water recirculating systems for rainbow trout culture. N Am J Aquacult 72(1):1–9. https://doi.org/10.1577/A09-009.1

    Article  Google Scholar 

  36. Rezanka T, Prell A, Sigler K (2008) Identification of odorous compounds from nine fermentor-cultivated Streptomyces strains. Folia Microbiol 53(4):315–318. https://doi.org/10.1007/s12223-008-0049-3

    Article  CAS  Google Scholar 

  37. Ichikawa N, Oguchi A, Ikeda H, Ishikawa J, Kitani S, Watanabe Y, Nakamura S, Katano Y, Kishi E, Sasagawa M, Ankai A, Fukui S, Hashimoto Y, Kamata S, Otoguro M, Tanikawa S, Nihira T, Horinouchi S, Ohnishi Y, Hayakawa M, Kuzuyama T, Arisawa A, Nomoto F, Miura H, Takahashi Y, Fujita N (2010) Genome sequence of Kitasatospora setae NBRC 14216T: an evolutionary snapshot of the family Streptomycetaceae. DNA Res 17(6):393–406. https://doi.org/10.1093/dnares/dsq026

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  38. Omura S, Takahashi Y, Iwai Y, Tanaka H (1982) Kitasatosporia, a new genus of the order Actinomycetales. J Antibiot 35(8):1013–1019. https://doi.org/10.7164/antibiotics.35.1013

    Article  CAS  Google Scholar 

  39. Schrader KK, Harries MD, Page PN (2015) Temperature effects on biomass, geosmin, and 2-methylisoborneol production and cellular activity by Nocardia spp. and Streptomyces spp. isolated from rainbow trout recirculating aquaculture systems. J Ind Microbiol Biotechnol 42(5):759–767. https://doi.org/10.1007/s10295-015-1600-2

    Article  PubMed  CAS  Google Scholar 

  40. Cane DE, He XF, Kobayashi S, Omura S, Ikeda H (2006) Geosmin biosynthesis in Streptomyces avermitilis. Molecular cloning, expression, and mechanistic study of the germacradienol/geosmin synthase. J Antibiot 59(8):471–479

    Article  CAS  Google Scholar 

  41. Jiang J, Cane DE (2008) Geosmin biosynthesis. Mechanism of the fragmentation-rearrangement in the conversion of germacradienol to geosmin. J Am Chem Soc 130(2):428–429. https://doi.org/10.1021/ja077792i

    Article  PubMed  CAS  Google Scholar 

  42. Jiang J, He X, Cane DE (2007) Biosynthesis of the earthy odorant geosmin by a bifunctional Streptomyces coelicolor enzyme. Nat Chem Biol 3(11):711–715. https://doi.org/10.1038/nchembio.2007.29

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  43. Jiang J, He X, Cane DE (2006) Geosmin biosynthesis. Streptomyces coelicolor germacradienol/germacrene D synthase converts farnesyl diphosphate to geosmin. J Am Chem Soc 128(25):8128–8129. https://doi.org/10.1021/ja062669x

    Article  PubMed  CAS  Google Scholar 

  44. Xu J, Wang Y, Xie SJ, Xu J, Xiao J, Ruan JS (2009) Streptomyces xiamenensis sp. Nov., isolated from mangrove sediment. J Syst Evol Microbiol 59(3):472–476. https://doi.org/10.1099/ijs.0.000497-0

    Article  CAS  Google Scholar 

  45. Peng C, Yan X, Wang X, Huang Y, Jiang L, Yuan P, Wu X (2020) Release of odorants from sediments of the largest drinking water reservoir in Shanghai: influence of pH, temperature, and hydraulic disturbance. Chemosphere 265:129068. https://doi.org/10.1016/j.chemosphere.2020.129068

    Article  PubMed  CAS  Google Scholar 

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Acknowledgements

This work was supported as commissioned research from Shimane prefecture (2017–2019). The authors would like to thank the Shimane prefecture kenou prefectural land maintenance office for providing information about odorous compounds in the Sanbe Reservoir. The authors thank the faculty of Life and Environmental Science at Shimane University for their financial support for the publication of this report. The authors would like to thank Editage (www.editage.jp) for English language editing.

Funding

This research was financially supported by Shimane prefecture.

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Authors and Affiliations

  1. Faculty of Life and Environmental Science, Shimane University, 1060 Nishikawatsu, Matsue, Shimane, 690-8504, Japan

    Shohei Hayashi

  2. Estuary Research Center, Shimane University, 1060 Nishikawatsu, Matsue, Shimane, 690-8504, Japan

    Shohei Hayashi, Shingo Masuki, Sangyeob Kim & Yasushi Seike

  3. Shimane Environment & Health Public Corporation, 1-4-6 Koshibara, Matsue, Shimane, 690-0012, Japan

    Koichi Furuta & Shinichi Doi

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  1. Shohei Hayashi
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Contributions

SH, SM, SK and YS designed the project and wrote the manuscript. SH designed and performed the isolation and genetic analysis. SH and SM collected water and sediment samples. KF and DS contributed to the analysis of geosmin and 2-MIB. All authors reviewed and approved the final manuscript.

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Correspondence to Shohei Hayashi.

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Hayashi, S., Masuki, S., Furuta, K. et al. Phylogenetic Analysis and Characterization of Odorous Compound-Producing Actinomycetes in Sediments in the Sanbe Reservoir, A Drinking Water Reservoir in Japan. Curr Microbiol 79, 344 (2022). https://doi.org/10.1007/s00284-022-03052-8

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