Microbial Production of the Off-Flavor Geosmin in Tilapia Production in Brazilian Water Reservoirs: Importance of Bacteria in the Intestine and Other Fish-Associated Environments

Mie B Lukassen; Nadieh de Jonge; Sabine M Bjerregaard; Raju Podduturi; Niels O G Jørgensen; Mikael A Petersen; Gianmarco S David; Reinaldo J da Silva; Jeppe L Nielsen

doi:10.3389/fmicb.2019.02447

Microbial Production of the Off-Flavor Geosmin in Tilapia Production in Brazilian Water Reservoirs: Importance of Bacteria in the Intestine and Other Fish-Associated Environments

Front Microbiol. 2019 Oct 31:10:2447. doi: 10.3389/fmicb.2019.02447. eCollection 2019.

Authors

Mie B Lukassen¹, Nadieh de Jonge¹, Sabine M Bjerregaard¹, Raju Podduturi², Niels O G Jørgensen², Mikael A Petersen³, Gianmarco S David⁴, Reinaldo J da Silva⁵, Jeppe L Nielsen¹

Affiliations

¹ Department of Chemistry and Bioscience, Aalborg University, Aalborg, Denmark.
² Department of Plant and Environmental Sciences, University of Copenhagen, Copenhagen, Denmark.
³ Department of Food Sciences, Section of Design and Consumer Behaviour, University of Copenhagen, Copenhagen, Denmark.
⁴ São Paulo State Agribusiness Technology at Jaú, Jaú, Brazil.
⁵ Departamento de Parasitologia, Instituto de Biociências, Universidade Estadual Paulista Júlio de Mesquita Filho, Botucatu, Brazil.

Abstract

Aim: To determine major sources of microbially produced geosmin in the commercially important aquaculture fish species tilapia.

Methods and results: Abundance and composition of geosmin-producing bacteria in water and fish biosphere (intestine, digesta, and fins) of Nile tilapia (Oreachromis niloticus) raised in net cages in Brazilian freshwater farms were examined. By combining qPCR of the geosmin synthase geoA gene and 16S rRNA gene amplicon sequencing to identify potential geosmin-producing organisms, we observed that the proportion and composition of geosmin producers appeared to be rather similar in the water, digesta, intestinal mucous, and on skin, making up about 0.1-0.2% of the total bacterial densities. A high proportion of Cyanobacteria and other putative geosmin producers affiliated to the Actinomycetales were identified in the intestinal mucous layer. The main uptake site for geosmin in fish is traditionally assumed to be through the gill surface, but the present results suggest that uptake by the intestinal tract may represent a major source of geosmin uptake in fish.

Conclusion: The high abundance of geosmin-producing bacteria in the intestinal mucous layer and digesta may indicate that the digestive system in fish is an important, but hitherto overlooked, source of geosmin and likely other off-flavors in fish.

Significance and impact of study: Tainting of fish by microbially produced off-flavors spoils fish quality and lowers consumer preferences for aquaculture-produced freshwater fish. Our results highlight the potential for the application of probiotic microorganisms for management of the intestinal microflora to improve the fish quality.

Highlights: -Off-flavor producing bacteria are widely abundant in aquaculture.-Off-flavor producers found on skin surface of fish.-Off-flavor producing bacteria accumulate in the digestive system.-Off-flavor producers might release significant amounts of off-flavor during lysis in the gut.-Off-flavor uptake through the digestive system might be quantitatively significant.

Keywords: Nile tilapia; aquaculture production; gastrointestinal tract; geoA; geosmin; off-flavor.