Deciphering microbial landscapes of fish eggs to mitigate emerging diseases

Yiying Liu; Irene de Bruijn; Allison Lh Jack; Keith Drynan; Albert H van den Berg; Even Thoen; Vladimir Sandoval-Sierra; Ida Skaar; Pieter van West; Javier Diéguez-Uribeondo; Menno van der Voort; Rodrigo Mendes; Mark Mazzola; Jos M Raaijmakers

doi:10.1038/ismej.2014.44

Deciphering microbial landscapes of fish eggs to mitigate emerging diseases

Yiying Liu, Irene de Bruijn, Allison Lh Jack, Keith Drynan, Albert H van den Berg, Even Thoen, Vladimir Sandoval-Sierra, Ida Skaar, Pieter van West, Javier Diéguez-Uribeondo, Menno van der Voort, Rodrigo Mendes, Mark Mazzola, Jos M Raaijmakers

Research output: Contribution to journal › Article › peer-review

60 Citations (Scopus)

Abstract

Animals and plants are increasingly suffering from diseases caused by fungi and oomycetes. These emerging pathogens are now recognized as a global threat to biodiversity and food security. Among oomycetes, Saprolegnia species cause significant declines in fish and amphibian populations. Fish eggs have an immature adaptive immune system and depend on nonspecific innate defences to ward off pathogens. Here, meta-taxonomic analyses revealed that Atlantic salmon eggs are home to diverse fungal, oomycete and bacterial communities. Although 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 Saprolegniato salmon eggs. These results highlight that fundamental insights into microbial landscapes of fish eggs may provide new sustainable means to mitigate emerging diseases.The ISME Journal advance online publication, 27 March 2014; doi:10.1038/ismej.2014.44.

Original language	English
Pages (from-to)	2002-2014
Number of pages	13
Journal	The ISME Journal
Volume	8
Issue number	10
Early online date	27 Mar 2014
DOIs	https://doi.org/10.1038/ismej.2014.44
Publication status	Published - Oct 2014

Bibliographical note

We are grateful to Menno ter Veld and Geert Wiegertjes (Animal Sciences, Wageningen University, The Netherlands) for their advice, help and valuable suggestions for the in vivo experiments. We thank the Laboratory of Jean Beagle Ristraino (North Carolina State University, USA) for the provision of genomic DNA extraction protocol for oomycete isolates. We thank Viviane Cordovez da Cunha (Wageningen University) for her help in culturing and characterization of Actinobacteria. This work was financially supported by SAPRO (Sustainable Approaches to Reduce Oomycete (Saprolegnia) Infections in Aquaculture), a Marie Curie Initial Training Network funded by the European Commission (EC) under Framework Program 7. Javier Diéguez-Uribeondo was supported by grant of MINECO CGL2012-39357. PhyloChip hybridizations and initial data analyses were performed at Second Genome, CA, USA. This manuscript is publication number 5586 of Netherlands Institute of Ecology (NIOO-KNAW).

Keywords

salmon
saprolegniosis
actinobacteria
microbiome
emerging pathogens

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

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10.1038/ismej.2014.44

Pieter van West
Person: Academic

Cite this

Liu, Y., de Bruijn, I., Jack, A. L., Drynan, K., van den Berg, A. H., Thoen, E., Sandoval-Sierra, V., Skaar, I., van West, P., Diéguez-Uribeondo, J., van der Voort, M., Mendes, R., Mazzola, M., & Raaijmakers, J. M. (2014). Deciphering microbial landscapes of fish eggs to mitigate emerging diseases. The ISME Journal, 8(10), 2002-2014. https://doi.org/10.1038/ismej.2014.44

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abstract = "Animals and plants are increasingly suffering from diseases caused by fungi and oomycetes. These emerging pathogens are now recognized as a global threat to biodiversity and food security. Among oomycetes, Saprolegnia species cause significant declines in fish and amphibian populations. Fish eggs have an immature adaptive immune system and depend on nonspecific innate defences to ward off pathogens. Here, meta-taxonomic analyses revealed that Atlantic salmon eggs are home to diverse fungal, oomycete and bacterial communities. Although 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 Saprolegniato salmon eggs. These results highlight that fundamental insights into microbial landscapes of fish eggs may provide new sustainable means to mitigate emerging diseases.The ISME Journal advance online publication, 27 March 2014; doi:10.1038/ismej.2014.44.",

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author = "Yiying Liu and {de Bruijn}, Irene and Jack, {Allison Lh} and Keith Drynan and {van den Berg}, {Albert H} and Even Thoen and Vladimir Sandoval-Sierra and Ida Skaar and {van West}, Pieter and Javier Di{\'e}guez-Uribeondo and {van der Voort}, Menno and Rodrigo Mendes and Mark Mazzola and Raaijmakers, {Jos M}",

note = "We are grateful to Menno ter Veld and Geert Wiegertjes (Animal Sciences, Wageningen University, The Netherlands) for their advice, help and valuable suggestions for the in vivo experiments. We thank the Laboratory of Jean Beagle Ristraino (North Carolina State University, USA) for the provision of genomic DNA extraction protocol for oomycete isolates. We thank Viviane Cordovez da Cunha (Wageningen University) for her help in culturing and characterization of Actinobacteria. This work was financially supported by SAPRO (Sustainable Approaches to Reduce Oomycete (Saprolegnia) Infections in Aquaculture), a Marie Curie Initial Training Network funded by the European Commission (EC) under Framework Program 7. Javier Di{\'e}guez-Uribeondo was supported by grant of MINECO CGL2012-39357. PhyloChip hybridizations and initial data analyses were performed at Second Genome, CA, USA. This manuscript is publication number 5586 of Netherlands Institute of Ecology (NIOO-KNAW).",

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AU - Drynan, Keith

AU - van den Berg, Albert H

AU - Thoen, Even

AU - Sandoval-Sierra, Vladimir

AU - Skaar, Ida

AU - van West, Pieter

AU - Diéguez-Uribeondo, Javier

AU - van der Voort, Menno

AU - Mendes, Rodrigo

AU - Mazzola, Mark

AU - Raaijmakers, Jos M

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N2 - Animals and plants are increasingly suffering from diseases caused by fungi and oomycetes. These emerging pathogens are now recognized as a global threat to biodiversity and food security. Among oomycetes, Saprolegnia species cause significant declines in fish and amphibian populations. Fish eggs have an immature adaptive immune system and depend on nonspecific innate defences to ward off pathogens. Here, meta-taxonomic analyses revealed that Atlantic salmon eggs are home to diverse fungal, oomycete and bacterial communities. Although 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 Saprolegniato salmon eggs. These results highlight that fundamental insights into microbial landscapes of fish eggs may provide new sustainable means to mitigate emerging diseases.The ISME Journal advance online publication, 27 March 2014; doi:10.1038/ismej.2014.44.

AB - Animals and plants are increasingly suffering from diseases caused by fungi and oomycetes. These emerging pathogens are now recognized as a global threat to biodiversity and food security. Among oomycetes, Saprolegnia species cause significant declines in fish and amphibian populations. Fish eggs have an immature adaptive immune system and depend on nonspecific innate defences to ward off pathogens. Here, meta-taxonomic analyses revealed that Atlantic salmon eggs are home to diverse fungal, oomycete and bacterial communities. Although 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 Saprolegniato salmon eggs. These results highlight that fundamental insights into microbial landscapes of fish eggs may provide new sustainable means to mitigate emerging diseases.The ISME Journal advance online publication, 27 March 2014; doi:10.1038/ismej.2014.44.

KW - salmon

KW - saprolegniosis

KW - actinobacteria

KW - microbiome

KW - emerging pathogens

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SN - 1751-7362

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JO - The ISME Journal

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ER -

Deciphering microbial landscapes of fish eggs to mitigate emerging diseases

Abstract

Bibliographical note

Keywords

UN SDGs

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Pieter van West

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