Deciphering microbial landscapes of fish eggs to mitigate emerging disease

Authors: LIU, YIYING - Wageningen University; DE BRUIJN, IRENE - Wageningen University; JACK, ALLISON - Wageningen University; DRYNAN, KEITH - Landcatch, Hendrix Genetices; VAN DEN BERG, HERBERT - Aberdeen Oomycete Laboratory; THOEN, EVEN - Norwegian Veterinary Institute; SANDOVAL-SIERRA, VLADIMIR - Real Jardin Bolancio Csic; SKAAR, IDA - Norwegian Veterinary Institute; VAN WEST, PIETER - Aberdeen Oomycete Laboratory; DIEGUEZ-URIBEONDO, JAVIER - Real Jardin Bolancio Csic; VAN DER VOORT, MENNO - Wageningen University; MENDES, RODRIGO - Embrapa; Mazzola, Mark; RAAIJMAKERS, JOS - Wageningen University

Submitted to: The ISME Journal: Multidisciplinary Journal of Microbial Ecology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 2/27/2014
Publication Date: 3/28/2014
Citation: Liu, Y., De Bruijn, I., Jack, A.L., Drynan, K., Van Den Berg, H., Thoen, E., Sandoval-Sierra, V., Skaar, I., Van West, P., Dieguez-Uribeondo, J., Van Der Voort, M., Mendes, R., Mazzola, M., Raaijmakers, J.M. 2014. Deciphering microbial landscapes of fish eggs to mitigate emerging disease. The ISME Journal: Multidisciplinary Journal of Microbial Ecology. 8:2001-2014.

Interpretive Summary: Fungal diseases that were previously not considered as major threats to ecosystem functioning are now causing severe ecological disruption. Saprolegniosis is a major disease problem in different wild and farmed fish species, including salmon. To control and prevent the spread of emerging pathogens, several conservation and disease mitigation strategies have been proposed because a singular solution is doubtful given the rich diversity of fish habitats. In these studies we deciphered the microbiome of Atlantic salmon eggs and determined how Saprolegniosis impacts the structure (richness, evenness) of fungal, oomycete and bacterial communities, with the ultimate goal to identify microorganisms that prevent or delay disease onset and/or development. Resistance of salmon eggs to disease development was associated with differences in the bacterial community supported by the salmon eggs. In particular, healthy eggs batches sustained an abundance of bacteria that belong to the genus Frondihabitans and these bacteria were shown to effectively inhibit development of the disease, Saprolegniosis. Given the importance of aquaculture for long-term food security, there is a strong need for sustainable means to mitigate Saprolegniosis and other emerging diseases. Our results provide a strong basis for the selection of beneficial microorganisms that can act as a first line of defense. Similar strategies can be used to mitigate other diseases including those that threaten wild populations of fish and amphibians.

Technical Abstract: Animals and plants are increasingly suffering from diseases caused by fungi and oomycetes. These emerging pathogens are now recognised as a global threat to biodiversity and food security. Amongst oomycetes, Saprolegnia species cause significant declines in fish and amphibian populations. Fish eggs have animmature adaptive immune system and depend on nonspecific innate defences toward off pathogens. Here, meta-taxonomic analyses revealed that Atlantic salmon eggs are home to diverse fungal, oomycete and bacterial communities. While virulent Saprolegnia isolates were found in all salmon egg samples, a low incidence of Saprolegniosis was strongly correlated with a high richness and abundance of specific commensal Actinobacteria, with the genus Frondihabitans (Microbacteriaceae) effectively inhibiting attachment of Saprolegnia to salmon eggs. These results highlight that fundamental insights into microbial landscapes of fish eggs may provide new sustainable means to mitigate emerging diseases.