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

Volumn 40, Issue 2, 2014, Pages 404-414

  Kutovaya, Olga A ^a   Watson, Sue B ^a  

^a ENVIRONMENT CANADA   (Canada)

Author keywords

Actinomycetes; Cyanobacteria; Geosmin; Geosmin synthase; Great Lakes; Taste odor

Indexed keywords

ASSAYS; BACTERIA; BIOCHEMISTRY; LAKES; LOSSES; POLYMERASE CHAIN REACTION; GENES; POTABLE WATER;

ACTINOMYCETES; CYANOBACTERIA; GEOSMIN; GREAT LAKES; SYNTHASES; TASTE-ODOR;

GENE EXPRESSION;

BACTERIUM; CYANOBACTERIUM; GENE EXPRESSION; MOLECULAR ANALYSIS; MONITORING; ODOR; PHYLOGENETICS; TEMPERATURE EFFECT; TERPENE; ASSAY; CONCENTRATION (COMPOSITION); DATABASE; DETECTION METHOD; ORGANIC COMPOUND; PHYTOPLANKTON; SEDIMENT ANALYSIS; TASTE;

GREAT LAKES [NORTH AMERICA];

ACTINOBACTERIA; ACTINOBACTERIA (CLASS); ANABAENA; CYANOBACTERIA; NOSTOCACEAE;

EID: 84901284435     PISSN: 03801330     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jglr.2014.03.016     Document Type: Article

References (75)

1. Agger S.A., Lopez-Gallego F., Hoye T.R., Schmidt-Dannert C. Identification of sesquiterpene synthases from Nostoc punctiforme PCC 73102 and Nostoc sp. strain PCC 7120. J. Bacteriol. 2008, 190:6084-6096.
2. Andersen R.A. Algal Culturing Techniques 2005, Elsevier Academic Press, San Diego, CA, USA, (578 pp.).
3. Anderson B.C., Quartermaine L.-K. Tastes and odours in Kingston's municipal drinking water: a case study of the problem and appropriate solutions. J. Great Lakes Res. 1998, 24:859-867.
4. Aoyama K., Kawamura N., Saitoh M., Magara Y., Ishibashi Y. Interactions between bacteria-free Anabaena macrospora clone and bacteria isolated from unialgal culture. Water Sci. Technol. 1995, 31(11):121-126.
5. Auffret M., Pilote A., Proulx E., Proulx D., Vandenberg G., Villemur R. Establishment of a real-time PCR method for quantification of geosmin-producing Streptomyces spp. in recirculating aquaculture systems. Water Res. 2011, 45:6753-6762.
6. Bafford R.A., Seagull R.W., Chung S.-Y., Millie D.F. Intracellular localization of the taste/odour metabolite 2-methylisoborneol in Oscillatoria limosa (Cyanophyta). J. Phycol. 1993, 29:91-95.
7. Bowmer K.H., Padovan A., Oliver R.L., Korth W., Ganf G.G. Physiology of geosmin production by Anabaena circinalis isolated from the Murrumbidgee River, Australia. Water Sci. Technol. 1992, 25:259-267.
8. Brittain S., Wang S., Babcock-Jackson L., Carmichael W., Rinehart K., Culver D. Isolation and characterization of microcystins, cyclic heptapeptide hepatotoxins from a Lake Erie strain of Microcystis aeruginosa. J. Great Lakes Res. 2001, 26:241-249.
9. Cane D.E., He X., Kobayashi S., Omura S., Ikeda H. Geosmin biosynthesis in Streptomyces avermitilis, molecular cloning, expression, and mechanistic study of the germacradienol/geosmin synthase. J. Antibiot. 2006, 59(8):471-479.
10. Chomczynski P., Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem. 1987, 162:156-159.
11. Cook D., Newcombe G., Sztajnbok P. The application of powdered activated carbon for MIB and geosmin removal: predicting PAC doses in four raw waters. Water Res. 2001, 35:1325-1333.
12. Dereeper A., Guignon V., Blanc G., Audic S., Buffet S., Chevenet F., Dufayard J.-F., Guindon S., Lefort V., Lescot M., Claverie J.-M., Gascuel O. Phylogeny.fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Res. 2008, 36(Web Server Issue):W465-W469.
13. Dzialowski A.R., Smith V.H., Huggins D.G. Development of predictive models for geosmin-related taste and odour in Kansas, USA, drinking water reservoirs. Water Res. 2009, 43:2829-2840.
14. Edwards U., Rogall T., Blöcker H., Emde M., Böttger E.C. Isolation and direct complete nucleotide determination of entire genes. Characterization of a gene coding for 16S ribosomal RNA. Nucleic Acids Res. 1989, 17(19):7843-7853.
15. Environment Canada Major ions and nutrients. Manual of Analytical Methods 1994, Vol. 1. Environmental Conservation Service - ECD. Canadian Communications Group, Toronto, Ontario, Canada.
16. Gerber N.N., Lechevalier H.A. Geosmin, an earthy-smelling substance isolated from actinomycetes. Appl. Microbiol. 1965, 13:935-938.
17. Giglio S., Jiang J., Saint C.P., Cane D.E., Monis P.T. Isolation and characterization of the gene associated with geosmin production in cyanobacteria. Environ. Sci. Technol. 2008, 42(21):8027-8232.
18. Giglio S., Chou W.K.W., Ikeda H., Cane D.E., Monis P.T. Biosynthesis of 2-methylisoborneol in cyanobacteria. Environ. Sci. Technol. 2011, 45(3):992-998.
19. Hanson T.R. Economic impact of off-flavor to the U.S. catfish industry. Off-flavors in Aquaculture 2003, 13-29. American Chemical Society, Washington, DC. A.M. Rimando, K.K. Schrader (Eds.).
20. Hartman W.L. Effects of exploitation, environmental changes, and new species on the fish habitats and resources of Lake Erie. Technical Report #22 1973, 26-27. Great Lakes Fishery Commission, Ann Arbor, Michigan.
21. Howgate P. Tainting of farmed fish by geosmin and 2-methyl-isoborneol: a review of sensory aspects and of uptake/depuration. Aquaculture 2004, 234:155-181.
22. Ilikchyan I.N., McKay R.M., Zehr J.P., Dyhrman S.T., Bullerjahn G.S. Detection and expression of the phosphonate transporter gene phnD in marine and freshwater picocyanobacteria. Environ. Microbiol. 2009, 11:1314-1324.
23. Izaguirre G., Taylor W.D. A Pseudanabaena species from Castaic Lake, California, that produces 2-methylisoborneol. Water Res. 1998, 32(5):1673-1677.
24. Izaguirre G., Taylor W.D. A guide to geosmin- and MIB-producing cyanobacteria in the United States. Water Sci. Technol. 2004, 49(9):19-24.
25. Izaguirre G., Taylor W.D., Pasek J. Off-flavor problems in two reservoirs, associated with planktonic Pseudanabaena species. Water Sci. Technol. 1999, 40(6):85-90.
26. Jensen S.E., Anders C.L., Goatcher L.J., Perley T., Kenefick S., Hrudey S.E. Actinomycetes as a factor in odour problems affecting drinking water from the North Saskatchewan River. Water Res. 1994, 28:1393-1401.
27. Jiang J., Cane D.E. Geosmin biosynthesis. Mechanism of the fragmentation-rearrangement in the conversion of germacradienol to geosmin. J. Am. Chem. Soc. 2008, 130:428-429.
28. Jiang J., He X., Cane D.E. Biosynthesis of the earthy odourant geosmin by a bifunctional Streptomyces coelicolor enzyme. Nat. Chem. Biol. 2007, 3:711-715.
29. Johansen J.R., Casamatta D.A. Recognizing cyanobacterial diversity through adoption of a new species paradigm. Algol. Stud. 2005, 117(1):71-93.
30. Jüttner F. Dynamics of the volatile organic substances associated with cyanobacteria and algae in a eutrophic shallow lake. Appl. Environ. Microbiol. 1984, 47(4):814-820.
31. Jüttner F., Höflacher B., Wurster K. Seasonal analysis of volatile organic biogenic substances (VOBS) in freshwater phytoplankton populations dominated by Dinobryon, Microcystis and Aphanizomenon. J. Phycol. 1986, 22:169-175.
32. Jüttner F. Physiology and biochemistry of odourous compounds from freshwater cyanobacteria and algae. Water Sci. Technol. 1995, 31:69-78.
33. Jüttner F., Watson S.B. Biochemical and ecological control of geosmin and 2-methylisoborneol in source-waters. Appl. Environ. Microbiol. 2007, 73(4):4395-4406.
34. Klausen C., Nicolaisen M.H., Strobel B.W., Warnecke F., Nielsen J.L., Jørgensen N.O.G. Abundance of actinobacteria and production of geosmin and 2-methylisoborneol in Danish streams and fish ponds. Appl. Environ. Microbiol. 2005, 52:265-278.
35. Komárek J. Problems in cyanobacterial taxonomy; implication for most common toxin producing species. Rapporti ISTISAN 2002, 6-43. Istituto Superiore di Sanitá, Roma. S. Melchiorre, E. Viaggiu, M. Bruno (Eds.).
36. Komárek J., Zapomělová E. Planktic morphospecies of the cyanobacterial genus Anabaena=subg. Dolichospermum - 1. Part: coiled types. Fottea 2007, 7(1):1-31.
37. Komárek J., Zapomělová E. Planktic morphospecies of the cyanobacterial genus Anabaena=subg. Dolichospermum - 2. Part: straight types. Fottea 2008, 8(1):1-14.
38. Kotai J. Instructions for preparation of modified nutrient solution Z8 for algae. Publication B-11/69 1972, Norwegian Institute for Water Research, Blindern, Oslo 3. Norway.
39. Kumar S., Nei M., Dudley J., Tamura K. MEGA: a biologist-centric software for evolutionary analysis of DNA and protein sequences. Brief. Bioinform. 2007, 9:299-306.
40. Kutovaya O.A., McKay R.M., Beall B., Wilhelm S.W., Kane D., Chaffin J., Bridgeman T., Bullerjahn G.S. Evidence against fluvial seeding of recurrent toxic blooms of Microcystis spp. in Lake Erie's western basin. Harmful Algae 2011, 15:71-77.
41. Ludwig F., Medger A., Bornick H., Opitz M., Lang K., Gottfert M., Roske I. Identification and expression analyses of putative sesquiterpene synthase genes in Phormidium sp. and prevalence of geoA-like genes in a drinking water reservoir. Appl. Environ. Microbiol. 2007, 73:6988-6993.
42. Lund J.W.G., Kipling C., Le Cren E.D. The inverted microscope method of estimating algal numbers and the statistical basis of estimations by counting. Hydrobiologia 1958, 11:143-170.
43. Makarewicz J.C. A lakewide comparison of zooplankton biomass and its species composition in Lake Erie, 1983-87. J. Great Lakes Res. 1993, 19(2):275-290.
44. Matsumoto A., Tsuchiya Y. Earthy-musty odour-producing cyanophytes isolated from five water areas in Tokyo. Water Sci. Technol. 1988, 20:179-183.
45. Medsker L.L., Jenkins D., Thomas J.F. Odourous compounds in natural waters. An earthy-smelling compound associated with blue-green algae and actinomycetes. Environ. Sci. Technol. 1968, 2:461-464.
46. Millie D.F., Fahnenstiel G.L., Bressie J.D., Pigg R.J., Rediske R.R., Klarer D.M., Tester P.A., Litake R.W. Late-summer phytoplankton in western Lake Erie (Laurentian Great Lakes): bloom distributions, toxicity, and environmental influences. Aquat. Ecol 2009, 10.1007/s10452-009-9238-7.
47. Moore L., Watson S.B. The Ontario Water Works Consortium: a functional model of source water management and understanding. Water Sci. Technol. 2007, 55(5):195-201.
48. Naes H., Post A.F. Transient states of geosmin, pigments, carbohydrates and proteins in continuous cultures of Oscillatoria brevis induced by changes in nitrogen supply. Arch. Microbiol. 1988, 150:333-337.
49. Naes H., Utkilen H., Post A.F. Geosmin production in the cyanobacterium Oscillatoria brevis. Arch. Microbiol. 1989, 151:407-410.
50. Nicholls K., Carney E. The phytoplankton of the Bay of Quinte, 1972-2008: point-source phosphorus loading control, dreissenid mussel establishment, and a proposed community reference. Aquat. Ecosyst. Health Manag. 2011, 14(1):33-43.
51. Nielsen J.L., Klausen C., Nielsen P., Burford M., Jorgensen N. Detection of activity among uncultured actinobacteria in a drinking water reservoir. FEMS Microbiol. Ecol. 2006, 55(3):432-438.
52. Nübel U., Garcia-Pichel F., Muyzer G. PCR primers to amplify 16S rRNA genes from cyanobacteria. Appl. Environ. Microbiol. 1997, 63:3327-3332.
53. Ouellette A.J.A., Handy S.M., Wilhelm S.W. Toxic Microcystis is widespread in Lake Erie: PCR detection of toxin genes and molecular characterization of associated cyanobacterial communities. Microb. Ecol. 2006, 51:154-165. 10.1007/s00248-004-0146-z.
54. Persson P.E. Odourous algal cultures in culture collections. Water Sci. Technol. 1988, 20:211-213.
55. Persson P.E. Cyanobacteria and off-flavours. Phycologia 1996, 35(6S):168-171.
56. Rajaniemi P., Hrouzek P., Kastovska K., Willame R., Rantala A., Hoffmann L., Komárek J., Sivonen K. Phylogenetic and morphological evaluation of the genera Anabaena, Aphanizomenon, Trichormus and Nostoc (Nostocales, Cyanobacteria). Int. J. Syst. Evol. Microbiol. 2005, 55:11-26.
57. Rinta-Kanto J.M., Ouellette A.J.A., Twiss M.R., Boyer G.L., Bridgeman T.B., Wilhelm S.W. Quantification of toxic Microcystis spp. during the 2003 and 2004 blooms in Western Lake Erie. Environ. Sci. Technol. 2005, 39:4198-4205.
58. Rosen B., MacLeod B., Simpson M. Accumulation and release of geosmin during the growth phases of Anabaena circinalis (Kütz.) Rabenhorst. Water Sci. Technol. 1992, 25:185-190.
59. Saadoun I., Schrader K.K., Blevins W.T. Environmental and nutritional factors affecting geosmin synthesis by Anabaena sp. Water Res. 2001, 35:1209-1218.
60. Schrader K., Dennis M.E. Cyanobacteria and earthy/musty compounds found in commercial catfish (Ictalurus punctatus) ponds in the Mississippi delta and Mississippi-Alabama blackland prairie. Water Res. 2005, 39(13):2807-2814.
61. Smith V.H., Sieber-Denlinger J., deNoyelles F., Campell S., Pan S., Randtke S.J., Blain G., Strasser V.A. Managing taste and odour problems in a eutrophic drinking water reservoir. Lake Reservoir Manage. 2002, 18(4):319-323.
62. Sugiura N., Nakano K. Causative microorganisms for musty odour occurrence in the eutrophic Lake Kasumigaura. Hydrobiologia 2000, 434:145-150.
63. Taylor W.D., Losee R.F., Torobin M., Izaguirre G., Sass D., Khiari D., Atasi K. Early Warning and Management of Surface Water Taste-and-odour Events 2006, AWWA Research Foundation, Denver, CO, (237 pp.).
64. Utkilen H.C., Froshaug M. Geosmin production and excretion in a planktonic and benthic Oscillatoria. Water Sci. Technol. 1992, 25(2):199-206.
65. Wang S.H., Dzialowski A.R., Lim N.C., Spotts W.W., Huggins D.G., deNoyelles F. Relationships between cyanobacterial production and the physical and chemical properties of a Midwestern reservoir, USA. Hydrobiologia 2005, 541(1):29-43.
66. Watson S.B. Cyanobacterial and eukaryotic algal odour compounds: signals or by-products? A review of their biological activity. Phycologia 2003, 42(4):332-350.
67. Watson S., Ridal J. Periphyton: a primary source of widespread and severe taste and odour. Water Sci. Technol. 2004, 49:33-39.
68. Watson S.B., Brownlee B., Satchwill T., Hargesheimer E.E. Quantitative analysis of trace levels of geosmin and MIB in source and drinking water using headspace SPME. Water Res. 2000, 34:2818-2828.
69. Watson S.B., Millard S., Burley M. Taste-odour and toxins in the Bay of Quinte. Project Quinte Monitoring Report #16 2005, Bay of Quinte RAP Restoration Council/Project Quinte, Trenton, Ontario, (164 pp.).
70. Watson S.B., Charlton M., Yerubandi R., Howell T., Brownlee B., Marvin C., Ridal J., Millard S. Off-flavour issues in large waterbodies: physics, chemistry and biology in concert. Water Sci. Technol. 2007, 55(5):1-8.
71. Watson S.B., Ridal J., Boyer G.L. Taste and odour and cyanobacterial toxins: impairment, prediction, and management in the Great Lakes. Can. J. Fish. Aquat. Sci. 2008, 65(8):1779-1796.
72. Wilhelm S.W., Bullerjahn G.S., Eldridge M.L., Rinta-Kanto J.M., Poorvin L., Bourbonniere R.A. Seasonal hypoxia and the genetic diversity of prokaryote populations in the central basin hypolimnion of Lake Erie: evidence for abundant cyanobacteria and photosynthesis. J. Great Lakes Res. 2006, 32:657-671.
73. Yagi M., Nakashima S., Muramoto S. Biological degradation of musty odour compounds, 2-methylisoborneol and geosmin, in a bio-activated carbon filter. Water Sci. Technol. 1988, 20:255-260.
74. Zaitlin B., Watson S.B. Actinomycetes in relation to taste and odour in drinking water: myths, tenets and truths. Water Res. 2006, 40:1741-1753.
75. Zaitlin B., Watson S.B., Ridal J., Satchwill T., Parkinson D. Actinomycetes in Lake Ontario: habitats and geosmin and MIB production. J. Am. Water Works Assoc. 2003, 95:113-118.