Abstract
The secondary metabolites geosmin and 2-methylisoborneol (MIB) are known to taint fish with an undesirable, earthy-muddy taste and odor. In an earlier study on a zero-discharge recirculating aquaculture system (RAS), it was found that geosmin and MIB were removed by microbial communities residing in sludge from the digestion basin of the system. In the present study, 16S amplicon sequencing was used to identify changes in relative abundances of bacterial taxa in geosmin and MIB-enriched crude sludge. The removal of geosmin and MIB by the sludge was accompanied by increased abundances of 12 operational taxonomic units (OTUs). The most prominent increase in abundances was recorded for OTUs affiliated with bacterial genera known to harbor denitrifiers. Among these were the Betaproteobacteria genera Thauera, which utilizes terpenes to fuel denitrification, and Comamonas, which was previously isolated from the digestion basin of the same system and is capable of growth on geosmin and MIB as sole carbon and energy sources. Thus far, denitrification has been associated with bacteria capable of utilizing terpenes other than geosmin and MIB. The significant increase in the abundance of denitrifying bacterial genera in sludge in which geosmin and MIB comprised only 0.06% of the total carbon content might indicate that such bacteria play a major role in the removal of these compounds in anoxic environments.
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References
Food and Agriculture Organization (FAO) (2018) The state of world fisheries and aquaculture 2018. Food and Agriculture Organization, Rome
van Rijn J (2013) Waste treatment in recirculating aquaculture systems. Aquac Eng 53:49–56
Guttman L, van Rijn J (2008) Identification of conditions underlying production of geosmin and 2-methylisoborneol in a recirculating system. Aquaculture 279:85–91
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. N Am J Aquac 72:1–9
Houle S, Schrader KK, Francois NR, Comeau Y, Kharoune M, Summerfelt ST (2016) Geosmin causes off-flavour in arctic char in recirculating aquaculture systems. Aquac Res 42:360–365
Burr GS, Wolters WR, Schrader KK, Summerfelt ST (2012) Impact of depuration of earthy-musty off-flavors on fillet quality of Atlantic salmon, Salmo salar, cultured in a recirculating aquaculture system. Aquac Eng 50:28–36
Brzuszkiewicz E, Thürmer A, Schuldes J et al (2016) Chemical taste taint accumulation in RAS farmed fish – a Fr 13 risk assessment demonstrated with geosmin (GSM) and 2-methylisoborneol (MIB) in barramundi (Lates calcarifer). Food Control 60:309–319–319. https://doi.org/10.1007/s00203-011-0725-6
Lukassen MB, Saunders AM, Sindilariu PD, Nielsen JL (2017) Quantification of novel geosmin-producing bacteria in aquaculture systems. Aquaculture 497:304–310. https://doi.org/10.1007/978-1-60327-999-4_11
Howgate P (2004) Tainting of farmed fish by geosmin and 2-methylisoborneol: a review of sensory aspects and of uptake/depuration. Aquaculture 234:155–181
Burgos L, Lehmann M, Simon D, Rodrigues de Andrade HH, Ribas de Abreu BR, Dreher-Nabinger D, Grivicich I, Berwanger-Juliano V, Rodrigues-Dihl R (2014) Agents of earthy-musty taste and odor in water: evaluation of cytotoxicity, genotoxicity and toxicogenomics. Sci Total Environ 490:679–685
Engle CR, Pound GL, van der Ploeg M (1995) The cost of off-flavor. J World Aquac Soc 26:297–306
Davidson J, Schrader K, Ruan E, Swift B, Aalhus J, Juarez M, Wolters W, Burr G, Good C, Summerfelt ST (2014) Evaluation of depuration procedures to mitigate the off-flavor compounds geosmin and 2-methylisoborneol from Atlantic salmon Salmo salar raised to market-size in recirculating aquaculture systems. Aquac Eng 61:27–34
Schram E, van Kooten T, van de Heu JM, Schrama JM, Verreth JAJ, Murk AJ (2017) Geosmin depuration from European eel (Anguilla anguilla) is not affected by the water renewal rate of depuration tanks. Aquac Res 48:4646–4655
Guttman L, van Rijn J (2009) 2-Methylisoborneol and geosmin uptake by organic sludge derived from a recirculating aquaculture system. Water Res 43:474–480
Azaria S, Nir S, van Rijn J (2017) Combined adsorption and degradation of the off-flavor compound 2-methylisoborneol in sludge derived from a recirculating aquaculture system. Chemosphere 169:69–77
Cytryn E, van Rijn J, Schramm A, Gieseke A, de Beer D, Minz D (2005) Identification of bacterial communities potentially responsible for oxic and anoxic sulfide oxidation in biofilters of a recirculating mariculture system. Appl Environ Microbiol 71:6134–6141
Krom MD, Ben David A, Ingall ED, Benning LG, Clerici S, Bottrell S, Davies C, Potts NJ, Mortimer RJG, van Rijn J (2014) Bacterially mediated removal of phosphorus and cycling of nitrate and sulfate in the waste stream of a “zero-discharge” recirculating mariculture system. Water Res 56:109–121
Guttman L, van Rijn J (2012) Isolation of bacteria capable of growth with 2-methylisoborneol and geosmin as the sole carbon and energy sources. Appl Environ Microbiol 78:363–370
APHA (1998) Standard methods for the examination of water and wastewater, 20th edn. American Public Health Association, American Water Works Association and Water Environmental Federation, Washington DC
Lloyd SW, Lea JM, Zimba PV, Grimm CC (1998) Rapid analysis of geosmin and 2-methylisoborneol in water using solid phase micro extraction procedures. Water Res 32:2140–2146
Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Huntley J, Fierer N, Owens SM, Betley J, Fraser L, Bauer M, Gormley N, Gilbert JA, Smith G, Knight R (2012) Ultra-high throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. ISME J 6:1621–1624
Moonsamy PV, Williams T, Bonella P, Holcomb CL, Höglund BN, Hillman G, Goodridge D, Turenchalk GS, Blake LA, Daigle DA, Simen BB, Hamilton A, May AP, Erlich HA (2013) High throughput HLA genotyping using 454 sequencing and the Fluidigm Access Array™ system for simplified amplicon library preparation. Tissue Antigens 81:141–149
Zheng J, Kobert K, Flouri T, Stamatakis A (2014) PEAR: a fast and accurate illumina paired-end read merger. Bioinformatics 30:614–620
Edgar RC (2010) Search and clustering orders of magnitude faster than blast. Bioinformatics 26:2460–2461
Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, Peplies J, Glöckner FO (2013) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 41:590–596
Parks DH, Tyson GW, Hugenholtz P, Beiko RG (2014) STAMP: statistical analysis of taxonomic and functional profiles. Bioinformatics 30:3123–3124
Harb M, Wei C-H, Wang N, Amy G, Hong P-Y (2016) Organic micropollutants in aerobic and anaerobic membrane bioreactors: changes in microbial communities and gene expression. Bioresour Technol 218:882–891
Phan HV, Hai FI, Zhang R, Kang J, Price WE (2016) Bacterial community dynamics in an anoxic-aerobic membrane bioreactor—impact on nutrient and trace organic contaminant removal. Int Biodeter Biodegr 109:61–72
Hochstein LI, Betlach M, Kritikos G (1984) The effect of oxygen on denitrification during steady-state growth of Paracoccus halodenitrificans. Arch Microbiol 137:74–78
Patureau D, Davison J, Bernet N, Moletta R (1994) Denitrification under various aeration conditions in Comamonas sp., strain SGLY2. FEMS Microbiol Ecol 14:71–78
Neef A, Zaglauer A, Meier H, Amann R, Lemmer H, Schleifer K-H (1996) Population analysis in a denitrifying sand filter: conventional and in situ identification of Paracoccus spp. in methanol-fed biofilms. Appl Environ Microbiol 62:4329–4339
Gumaelius L, Magnusson G, Pettersson B, Dalhammer G (2001) Comamonas denitrificans sp. nov., an efficient denitrifying bacterium isolated from activated sludge. Int J Syst Evol Microbiol 51:999–1006
Xing D, Cheng S, Logan BE, Regan JM (2010) Isolation of the exoelectrogenic denitrifying bacterium Comamonas denitrificans based on dilution to extinction. Appl Microbiol Biotechnol 85:1575–1587
Adav SS, Lee D-J, Lai JY (2010) Microbial community of acetate utilizing denitrifiers in aerobic granules. Appl Microbiol Biotechnol 85:753–762
Grant MA, Payne WJ (1981) Denitrification by strains of Neisseria, Kingella, and Chromobacterium. Int J Syst Bacteriol 31:276–279
Bazylinski DA, Palome E, Blakemore NA, Blakemore RP (1986) Denitrification by Chromobacterium violaceum. Appl Environ Microbiol 52:696–699
van Rijn J, Tal Y, Barak Y (1996) Influence of volatile fatty acids on nitrite accumulation by a Pseudomonas stutzeri strain isolated from a denitrifying fluidized bed reactor. Appl Environ Microbiol 62:2615–2620
Tanaka A, Oritani T, Uehara F, Saito A, Kishita H, Niizeki Y, Fuchigami K (1996) Biodegradation of a musty odour component, 2-methylisoborneol. Water Res 30:759–761
Lauderdale CV, Aldrich HC, Lindner AS (2004) Isolation and characterization of a bacterium capable of removing taste- and odor-causing 2-methylisoborneol from water. Water Res 38:4135–4142
Eaton RW, Sandusky P (2010) Biotransformations of (+/−)-geosmin by terpene-degrading bacteria. Biodegradation 21:71–79
Harder J, Probian C (1995) Microbial degradation of monoterpenes in the absent of molecular oxygen. Appl Environ Microbiol 61:3804–3808
Pavlostathis SG, Misra G (1999) Biotransformation of selected monoterpenes under nitrate-reducing conditions. Appl Microbiol Biotechnol 53:63–68
Heyen H, Harder J (2000) Geranic acid formation, an initial reaction of anaerobic monoterpene metabolism in denitrifying Alcaligenes defragrans. Appl Environ Microbiol 66:3004–3009
Marmulla R, Cala EP, Markert S, Schweder T, Harder J (2016) The anaerobic linalool metabolism in Thauera linaloolentis 47 Lol. BMC Microbiol 16:76–84
Foss S, Harder J (1998) Thauera linaloolentis sp. nov. and Thauera terpenica sp. nov., isolated on oxygen-containing monoterpenes (linalool, menthol, and eucalyptol) and nitrate. Syst Appl Microbiol 21:365–373
Liu B, Zhang F, Feng X, Liu Y, Yan X, Zhang X, Wang L, Zhao L (2006) Thauera and Azoarcus as functionally important genera in a denitrifying quinoline-removal bioreactor as revealed by microbial community structure comparison. FEMS Microbiol Ecol 55:274–286
Shinoda Y, Sakai Y, Uenishi H, Uchihashi Y, Hiraishi A, Yukawa H, Yurimoto H, Kat N (2004) Aerobic and anaerobic toluene degradation by a newly isolated denitrifying bacterium, Thauera sp. strain DNT-1. Appl Environ Microbiol 70:1385–1392
Cytryn E, Gelfand I, Minz D, Neori A, Gieseke A, de Beer D, van Rijn J (2005) Sulfide-oxidizing activity and bacterial community structure in a fluidized bed reactor from a zero-discharge mariculture system. Environ Sci Technol 39:1802–1810
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This research was supported by research grant no. IS-4670-13R from BARD, The United States-Israel Binational Agricultural Research and Development Fund to JvR and AFP.
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Azaria, S., Post, A.F. & van Rijn, J. Changes in the Bacterial Community Structure of Denitrifying Sludge from a Recirculating Aquaculture System (RAS) After Geosmin and 2-Methylisoborneol Enrichment. Curr Microbiol 77, 353–360 (2020). https://doi.org/10.1007/s00284-019-01844-z
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DOI: https://doi.org/10.1007/s00284-019-01844-z