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Microbial Organic Compounds Generating Taste and Odor in Water

  • Dharumadurai Dhanasekaran
  • Saravanan Chandraleka
  • Govindhan Sivaranjani
  • Selvanathan Latha
Chapter
Part of the Environmental Chemistry for a Sustainable World book series (ECSW, volume 22)

Abstract

Odor compounds are mainly due to the presence of many volatile and semivolatile components with diverse chemical and physicochemical properties. These compounds are generally present within complex matrices. Odorous compounds in the soil have been subjected to scientific analysis for the determination of odor compounds produced by microorganisms. These compounds are also known as volatile organic compounds (VOCs). They are present in natural sources such as soil, air, freshwater, and marine water ecosystems, and they produce unpleasant musty odors or earthy odors.

VOCs have been isolated from Actinobacteria species, and these compounds play main roles in biological function. Common VOCs are alkanes, alkenes, alcohols, esters, ketones, sulfur compounds, and isoprenoid compounds. Geosmin and 2-methyl-isoborneol are naturally occurring compounds that have a very strong earthy taste and odor, and they can be simply detected by the human nose. Little is known about the fundamentals of microbial volatile odor compounds that contribute undesirable tastes or odors in water, soil, and aquaculture products. To address this knowledge gap, we have investigated the microbial community causing undesirable odors and tastes in water. The present review describes the microbial origin of odor compounds, particularly those caused by Actinobacteria. It also describes their distribution, occurrence, and chemical nature; detection of odor compounds; and biological methods used to remove undesirable odors from water.

Keywords

Streptomyces Odor compounds Geosmin Water odor and taste 

Notes

Acknowledgements

D.D. thanks the University Grants Commission (UGC), New Delhi, India, for financial support under the Raman Fellowship for Postdoctoral Research in the USA (F. no. 5-29/2016(IC) Dt.10.02.2016) and the Department of Science & Technology–Fund for Improvement of Science & Technology Infrastructure (DST-FIST) Programme (ref. no. SR/FIST/LS1-013/2012) dated August 13, 2012. S.L. is indebted to the Department of Science and Technology–Innovation in Science Pursuit for Inspired Research (DST-INSPIRE), New Delhi, India, for financial support in the form of a Junior and Senior Research Fellowship (DST Award Letter no. IF110317/DST/INSPIRE Fellowship/2011/Dt.29.06.2011).

References

  1. Adams BA (1929) Odours in the water of the Nile River. J Water Process Eng 31:309–314Google Scholar
  2. Amaral JA, Knowles R (1997) Inhibition of methane consumption in forest soils and pure cultures of methanotrophs by aqueous forest soil extracts. Soil Biol Biochem 29:1713–1720.  https://doi.org/10.1016/S0038-0717(97)00070-9 CrossRefGoogle Scholar
  3. Bays LR, Burman NP, Lewis WM (1970) Taste and odour in water supplies in Great Britain: a survey of the present position and problems for the future. Water Treat Exam 19(2):136–160Google Scholar
  4. Bennett JW, Inamdar AA (2015) Are some fungal volatile organic compounds (VOCs) mycotoxins? Toxins 7:3785–3804.  https://doi.org/10.3390/toxins7093785 CrossRefGoogle Scholar
  5. Bentley R, Meganathan R (1981) Geosmin and methylisoborneol biosynthesis in streptomycetes: evidence for an isoprenoid pathway and its absence in non-differentiating isolates. FEBS Lett 125(2):220–222.  https://doi.org/10.1016/0014-5793(81)80723-5 CrossRefGoogle Scholar
  6. Blevins WT, Schrader KK, Saadoun I (1995) Comparative physiology of geosmin production by Streptomyces halstedii and Anabaena sp. Water Sci Technol 31(11):127–133.  https://doi.org/10.1016/0273-1223(95)00466-Z CrossRefGoogle Scholar
  7. Bunge M, Araghipour N, Mikoviny T, Dunkl J, Schnitzhofer R, Hansel A, Schinner F, Wisthaler A, Margesin R, Mark TD (2008) On-line monitoring of microbial volatile metabolites by proton transfer reaction-mass spectrometry. Appl Environ Microbiol 74:2179–2186.  https://doi.org/10.1128/AEM.02069-07 CrossRefGoogle Scholar
  8. Burgos L, Lehmann M, de HHR A, de BRR A, de Souza AP, Juliano VB, Dihl RR (2014) In vivo and in vitro genotoxicity assessment of 2-methylisoborneol, causal agent of earthy–musty taste and odour in water. Ecotox Environ Safety 100:282–286.  https://doi.org/10.1371/journal.pone.0120675 CrossRefGoogle Scholar
  9. Cane DE, Watt RM (2003) Expression and mechanistic analysis of a germacradienol synthase from Streptomyces coelicolor implicated in geosmin biosynthesis. Proc Natl Acad Sci 100(4):1547–1551.  https://doi.org/10.1073/pnas.0337625100 CrossRefGoogle Scholar
  10. Chater KF et al (2002) Streptomyces coelicolor A3(2): from genome sequence to function. Methods Microbiol 33:321–336.  https://doi.org/10.1016/S0580-9517(02)33018-6 Google Scholar
  11. Davis TS, Crippen TL, Hofstetter RW et al (2013) Microbial volatile emissions as insect semiochemicals. J Chem Ecol 39:840–859.  https://doi.org/10.1007/s10886-013-0306-z CrossRefGoogle Scholar
  12. Dionigi CP, Millie DF, Spanier AM, Johnsen PB (1992) Spore and geosmin production by Streptomyces tendae on several media. J Agric Food Chem 40(1):122–125.  https://doi.org/10.1021/jf00013a023 CrossRefGoogle Scholar
  13. Elhadi SL, Huck PM, Slawson RM (2004) Removal of geosmin and 2-methylisoborneol by biological filtration. Water Sci Technol 49(9):273–280CrossRefGoogle Scholar
  14. Elhadi SL, Huck PM, Slawson RM (2006) Factors affecting the removal of geosmin and MIB in drinking water biofilters. J Am Water Works Assoc 98:108–120CrossRefGoogle Scholar
  15. Forbes SL, Perrault KA (2014) Decomposition odour profiling in the air and soil surrounding vertebrate carrion. PLoS One 9(4):e95107.  https://doi.org/10.1371/journal.pone.0095107 CrossRefGoogle Scholar
  16. Friedrich J, Watson SB (2007) Biochemical and ecological control of geosmin and 2-methylisoborneol in source waters. Appl Environ Microbiol 73:4395–4406.  https://doi.org/10.1128/AEM.02250-06 CrossRefGoogle Scholar
  17. Gaines HD, Collins RP (1963) Volatile substances produced by Streptomyces odourifer. Lloydia 26(4):247Google Scholar
  18. Gerber NN (1967) Geosmin, an earthy smelling substance isolated from actinomycetes. Biotechnol Bioeng 9:321CrossRefGoogle Scholar
  19. Gerber NN (1969) A volatile metabolite of actinomycetes, 2-methylisoborneol. J Antibiot 22(10):508–509CrossRefGoogle Scholar
  20. Gerber NN (1979) Volatile substances from actinomycetes: their role in the odor pollution of water. CRC Crit Rev Microbiol 7:191CrossRefGoogle Scholar
  21. Gerber NN, Lechevalier HA (1965) Geosmin, an earthy-smelling substance isolated from actinomycetes. Appl Microbiol 13(6):935–938Google Scholar
  22. Goodfellow M, Williams ST (1983) Ecology of actinomycetes. Annu Rev Microbiol 37(1):189–216CrossRefGoogle Scholar
  23. Gust B, Challis GL, Fowler K, Kieser T, Chater KF (2003) PCR-targeted Streptomyces gene replacement identifies a protein domain needed for biosynthesis of the sesquiterpene soil odour geosmin. Proc Natl Acad Sci 100(4):1541–1546.  https://doi.org/10.1073/pnas.0337542100 CrossRefGoogle Scholar
  24. Howgate P (2004) Tainting of farmed fish by geosmin and 2-methyl-iso-borneol: a review of sensory aspects and of uptake/depuration. Aquaculture 234:155–181.  https://doi.org/10.1016/j.aquaculture.2003.09.032 CrossRefGoogle Scholar
  25. Huck PM, Kenefick SL, Hrudey SE, Zhang S (1995) Bench scale determination of the removal of odour compounds with biological treatment. Water Sci Technol 31:203–209.  https://doi.org/10.1016/0273-1223(95)00477-5 CrossRefGoogle Scholar
  26. Issatchenko B, Egorova A (1944) Actinomycetes in reservoirs as one of the causes responsible for the earthy smell of their waters. Mikrobiolgiya 13:224–230Google Scholar
  27. Jiang CL, Xu LH (1996) Diversity of aquatic actinomycetes in lakes of the Middle Plateau, Yunnan, China. Appl Environ Microbiol 62(1):249–253Google Scholar
  28. Jiang J, He X, Cane DE (2007) Biosynthesis of the earthy odourant geosmin by a bifunctional Streptomyces coelicolor enzyme. Nat Chem Biol 3(11):711–715.  https://doi.org/10.1038/nchembio.2007.29 CrossRefGoogle Scholar
  29. Jung SW, Baek KH, Yu MJ (2004) Treatment of taste and odor material by oxidation and adsorption. Water Sci Technol 49:289–295CrossRefGoogle Scholar
  30. Juttner F, Watson SB (2007) Biochemical and ecological control of geosmin and 2-methylisoborneol in source waters. Appl Environ Microbiol 73:4395–4406.  https://doi.org/10.1128/AEM.02250-06 CrossRefGoogle Scholar
  31. Kikuchi T, Mimura T, Harimaya K, Yano H, Arimoto T, Masada Y, Inoue K (1973) Odorous metabolites of actinomycetes biwako-C and -D strain isolated from the bottom deposits of Lake Biwa: identification of geosmin, methylisoborneol and furfural. Chem Pharm Bull 21:2339CrossRefGoogle Scholar
  32. 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 Microbio Eco 52(2):265–278CrossRefGoogle Scholar
  33. Koch B, Gramith JT, Dale MS, Ferguson DW (1992) Control of 2-methylisoborneol and geosmin by ozone and peroxone—a pilot study. Water Sci Technol 25(2):291–298CrossRefGoogle Scholar
  34. Komatsu M, Tsuda M, Omura S, Oikawa H, Ikeda H (2008) Identification and functional analysis of genes controlling biosynthesis of 2-methylisoborneol. Proc Natl Acad Sci 105(21):7422–7427.  https://doi.org/10.1073/pnas.0802312105 CrossRefGoogle Scholar
  35. Lalezary S, Pirbazari M, McGuire MJ (1986) Oxidation of five earthy–musty taste and odor compounds. J Am Water Works Assoc 8:62–69CrossRefGoogle Scholar
  36. Leff JW, Fierer N (2008) Volatile organic compound (VOC) emissions from soil and litter samples. Soil Biol Biochem 40:1629–1636.  https://doi.org/10.1016/j.soilbio.2008.01.018 CrossRefGoogle Scholar
  37. Lloyd SW, Grimm CC (1999) Analysis of 2-methylisoborneol and geosmin in catfish by microwave distillation-solid-phase microextraction. J Agric Food Chem 47(1):164–169.  https://doi.org/10.1021/jf980419x CrossRefGoogle Scholar
  38. Lovell RT (1983) New off-flavors in pond-cultured channel catfish. Aquaculture 30:329–334CrossRefGoogle Scholar
  39. Lundgren BV, Grimvall A, Savenhed R (1988) Formation and removal of off-flavor compounds during ozonation and filtration through biologically-active sand filters. Water Sci Technol 20(8–9):245–253CrossRefGoogle Scholar
  40. Mackie AE, Wheatley RE (1999) Effects and incidence of volatile organic compound interactions between soil bacterial and fungal isolates. Soil Biol Biochem 31:375–385.  https://doi.org/10.1016/S0038-0717(98)00140-0 CrossRefGoogle Scholar
  41. Maga JA (1987) Musty/earthy aromas. J Int Food Rev 3:269–284CrossRefGoogle Scholar
  42. Mayrhofer S, Mikoviny T, Waldhuber S, Wagner AO, Innerebner G, Frank-Whittle IH, Mark TD, Hansel A, Insam H (2006) Microbial community related to volatile organic compound (VOC) mission in household biowaste. Environ Microbiol 8:1960–1974.  https://doi.org/10.1111/j.1462-2920.2006.01076 CrossRefGoogle Scholar
  43. McGuire MJ, Krasner SW, Hwang CJ, Izaguirre G (1981) Closed-loop stripping analysis as a tool for solving taste and odor problems. J Am Water Works Assoc 73(10):530–537CrossRefGoogle Scholar
  44. Medsker LL, Jenkins D, Thomas JF (1968) Odorous compounds in natural waters: an earthy-smelling compound associated with blue-green algae and actinomycetes. Environ Sci Technol 2:461CrossRefGoogle Scholar
  45. Medsker LL, Jenkins D, Thomas JF, Koch C (1969) Odorous compounds in natural waters: 2 exo-hydroxy-2-methylbornate, the major odorous compound produced by actinomycetes. Environ Sci Technol 3:476CrossRefGoogle Scholar
  46. Nakajima M, Ogura T, Kusama Y, Iwabuchi N, Imawaka T, Araki A, Sunairi M (1996) Inhibitory effects of odour substances, geosmin and 2-methylisoborneol, on early development of sea urchins. Water Res 30(10):2508–2511.  https://doi.org/10.1016/0043-1354(96)00104-2 CrossRefGoogle Scholar
  47. Nerenberg R, Rittmann BE, Soucie WJ (2000) Ozone/biofiltration for removing MIB and geosmin. J Am Water Works Assoc 92:85–97CrossRefGoogle Scholar
  48. Nielsen JL, Klausen C, Nielsen PH, Burford M, Jorgensen NO (2006) Detection of activity among uncultured Actinobacteria in a drinking water reservoir. FEMS Microbiol Ecol 55(3):432–438.  https://doi.org/10.1111/j.1574-6941.2005.00054.x CrossRefGoogle Scholar
  49. Paavolainen L, Kitunen V, Smolander A (1998) Inhibition of nitrification in forest soil by monoterpenes. Plant Soil 205:147–154CrossRefGoogle Scholar
  50. Petersen MA, Hyldig G, Strobel BW, Henriksen NH, Jorgensen NOG (2011) Chemical and sensory quantification of geosmin and 2-methylisoborneol in rainbow trout (Oncorhynchus mykiss) from recirculated aquacultures in relation to concentrations in basin water. J Agric Food Chem 59:12561–12568.  https://doi.org/10.1021/jf2033494 CrossRefGoogle Scholar
  51. Petersen MA, Alam MA, Rahman MM, Ali ML, Mahmud S, Schluter L, Jorgensen NGO (2014) Geosmin off-flavour in pond-raised fish in southern Bangladesh and occurrence of potential off-flavour producing organisms. Aqua Environ Inter 5:107–116.  https://doi.org/10.3354/aei00100 CrossRefGoogle Scholar
  52. Piechulla B, Degenhardt J (2014) The emerging importance of microbial volatile organic compounds. Plant Cell Environ 37:811–812.  https://doi.org/10.1111/pce.12254 CrossRefGoogle Scholar
  53. Piet GJ, Zoeteman BCJ, Kraayeveld AJA (1972) Earthy smelling substances in surface waters of the Netherlands. Wat Treat Exam 21:281Google Scholar
  54. Rashash D, Dietrich A, Hoehn R (1997) Flavor profile analysis of selected odorous compounds. J Am Water Works Assoc 89(2):131–142CrossRefGoogle Scholar
  55. Robertson RF, Jauncey K, Beveridge MCM, Lawton LA (2005) Depuration rates and the sensory threshold concentration of geosmin responsible for earthy–musty taint in rainbow trout, Onchorynchus mykiss. Aquaculture 245:89–99CrossRefGoogle Scholar
  56. Rosen AA, Safferman RS, Mashni CI, Romano AH (1968) Identity of odorous substances produced by Streptomyces griseoluteus. Appl Microbiol 16:178Google Scholar
  57. Rosen AA, Mashni CI, Safferman RS (1970) Recent developments in the chemistry of odor in water: the cause of earthy/musty odor. Wat Treat Exam 19:106Google Scholar
  58. Scholler CE, Gurtler H, Pedersen R, Molin S, Wilkins K (2002) Volatile metabolites from actinomycetes. J Agric Food Chem 50(9):2615–2621.  https://doi.org/10.1021/jf0116754 CrossRefGoogle Scholar
  59. Schrader KK, Blevins WT (1993) Geosmin producing species of Streptomyces and Lyngbya from aquaculture ponds. Can J Microbiol 39:834–840.  https://doi.org/10.1139/m93-124 CrossRefGoogle Scholar
  60. Schrader KK, Blevins WT (1999) Effects of selected environmental conditions on biomass and geosmin production by Streptomyces halstedii. J Microbiol 37(3):159–167Google Scholar
  61. Schrader KK, Blevins WT (2001) Effects of carbon source, phosphorus concentration, and several micronutrients on biomass and geosmin production by Streptomyces halstedii. J Indus Microbio Biotech 26(4):241–247CrossRefGoogle Scholar
  62. Schrader K, Rubio SA, Piedrahita RH, Rimando AM (2005) Geosmin and 2-Methylisoborneol cause offflavors in cultured largemouth bass and white sturgeon reared in recirculating-water systems. N Am J Aquac 67(3):177–180.  https://doi.org/10.1577/A04-070.1.CrossRefGoogle Scholar
  63. Schrader KK, Summerfelt ST (2010) Distribution of off-flavor compounds and isolation of geosmin-producing bacteria in a series of water recirculating systems for rainbow trout culture. North Am J Aquacul 72(1):1–9.  https://doi.org/10.1577/A09-009.1 CrossRefGoogle Scholar
  64. Simons P (2003) Camels act on a hump. The Guardian. http://www.guardian.co.uk/science/2003/mar/06/science.research/print.
  65. Singh B, Oh TJ, Sohng JK (2009) Exploration of geosmin synthase from Streptomyces peucetius ATCC 27952 by deletion of doxorubicin biosynthetic gene cluster. J Indus Microbio Biotech 36(10):1257–1265.  https://doi.org/10.1007/s10295-009-0605-0 CrossRefGoogle Scholar
  66. Stotzky G, Schenck S (1976) Volatile organic compounds and microorganisms. CRC Crit Rev 4:333–381CrossRefGoogle Scholar
  67. Sugiura N, Nakano K (2000) Causative microorganisms for musty odor occurrence in the eutrophic Lake Kasumigaura. Hydrobiologia 434(1–3):145–150CrossRefGoogle Scholar
  68. Sunesson AL, Nilsson CA, Carlson R, Blomquist G, Andersson B (1997) Production of volatile metabolites from Streptomyces albidoflavus cultivated on gypsum board and tryptone glucose extract agar—influence of temperature, oxygen and carbon dioxide levels. Ann Occup Hyg 41(4):393–413CrossRefGoogle Scholar
  69. Thaysen AC (1936) The origin of an earthy or muddy taint in fish. Ann Appl Biol 23(1):99–104CrossRefGoogle Scholar
  70. Tucker CS (2000) Off-flavor problems in aquaculture. Rev Fish Sci 8:45–48.  https://doi.org/10.1080/10641260091129170 CrossRefGoogle Scholar
  71. Tung S, Lin T, Tseng I, Lin H (2006) Identification of 2-MIB and geosmin producers in Feng-Shen reservoir in south Taiwan. Water Supply 6(2):55–61CrossRefGoogle Scholar
  72. Warneke C, Karl T, Judmaier H, Hansel A, Jordan A, Lindinger W, Crutzen PJ (1999) Acetone, methanol, and other partially oxidized volatile organic emissions from dead plant 15 matter by a biological processes: significance for atmospheric HOx chemistry. Global Biogeochem Cy 13:9–17CrossRefGoogle Scholar
  73. Watson SB (2003) Cyanobacterial and eukaryotic algal odour compounds: signals or by-products. A review of their biological activity. Phycologia 42(4):332–350.  https://doi.org/10.2216/i0031-8884-42-4-332.1 CrossRefGoogle Scholar
  74. Watson SB, Cruz-Rivera E (2003) Algal chemical ecology: an introduction to the special issue. Phycologia 42(4):319–323.  https://doi.org/10.2216/i0031-8884-42-4-319.1 CrossRefGoogle Scholar
  75. Watson SB, Brownlee B, Satchwill T, Hargesheimer EE (2000) Quantitative analysis of trace levels of geosmin and MIB in source and drinking water using headspace SPME. Water Res 34(10):2818–2828.  https://doi.org/10.1016/S0043-1354(00)00027-0 CrossRefGoogle Scholar
  76. Wenke K, Weise T, Warnke R et al (2012) Bacterial volatiles mediating information between bacteria and plants. In: Witzany G, Baluska F (eds) Biocommunication of plants, Signaling and communication in plants, vol 14. Springer, Berlin, pp 327–347CrossRefGoogle Scholar
  77. Wohl DL, Vaun McArthur J (1998) Actinomycete-flora associated with submersed freshwater macrophytes. FEMS Microbiol Ecol 26(2):135–140.  https://doi.org/10.1111/j.1574-6941.1998.tb00499.x CrossRefGoogle Scholar
  78. Wood S, Williams ST, White WR (1985) Potential sites of geosmin production by streptomycetes in and around reservoirs. J Appl Bact 58(3):319–326CrossRefGoogle Scholar
  79. Yagi O, Sugiura N, Sudo R (1987) Chemical and physical factors in the production of musty odour by Streptomyces spp. isolated from Lake Kasumigaura. Agric Biol Chem 51(8):2081–2088Google Scholar
  80. Yamprayoon J, Noomhorm A (2000) GSM and off-flavour in Nile tilapia (Oreochromis niloticus). J Aquat Food Prod Technol 9:29–41.  https://doi.org/10.1300/J030v09n02_04 CrossRefGoogle Scholar
  81. Young WF, Horth H, Crane R, Ogden T, Arnott M (1996) Taste and odour threshold concentrations of potential potable water contaminants. Water Res 30(2):331–340.  https://doi.org/10.1016/0043-1354(95)00173-5 CrossRefGoogle Scholar
  82. Young IM, Crawford JW, Nunan N, Otten W, Spiers A (2008) Microbial distribution in soils: physics and scaling. In: Sparks DL (eds) Advances in agronomy, vol 100. Elsevier Academic Press Inc, San Diego, pp 81–121Google Scholar
  83. Zacheus OM, Lehtola MJ, Korhonen LK, Martikainen PJ (2001) Soft deposits, the key site for microbial growth in drinking water distribution networks. Water Res 35(7):1757–1765.  https://doi.org/10.1016/S0043-1354(00)00431-0 CrossRefGoogle Scholar
  84. 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 CrossRefGoogle Scholar
  85. Zaitlin B, Watson SB, Ridal J, Satchwill T, Parkinson D (2003) Actinomycetes in Lake Ontario: habitats and geosmin and MIB production. J Am Water Works Assoc 95:113–118CrossRefGoogle Scholar
  86. Zuo Y, Li L, Wu Z, Song L (2009) Isolation, identification and odour-producing abilities of geosmin/2-MIB in actinomycetes from sediments in Lake Lotus. China J Water Supply Res Tech 58(8):552–561CrossRefGoogle Scholar
  87. Zuo Y, Li L, Zhang T, Zheng L, Dai G, Liu L, Song L (2010) Contribution of Streptomyces in sediment to earthy odour in the overlying water in Xionghe Reservoir, China. Water Res 44(20):6085–6094.  https://doi.org/10.1016/j.watres.2010.08.001 CrossRefGoogle Scholar

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Authors and Affiliations

  • Dharumadurai Dhanasekaran
    • 1
    • 2
  • Saravanan Chandraleka
    • 3
  • Govindhan Sivaranjani
    • 1
  • Selvanathan Latha
    • 1
  1. 1.Department of Microbiology, School of Life SciencesBharathidasan UniversityTiruchirappalliIndia
  2. 2.Department of Molecular, Cellular and Biomedical SciencesUniversity of New HampshireDurhamUSA
  3. 3.Department of ChemistryUrumu Dhanalakshmi CollegeTiruchirappalliIndia

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