Host-gut microbiota interactions shape parasite infections in farmed Atlantic salmon.

Autor:	Brealey JC; Department of Natural History, NTNU University Museum, Norwegian University of Science and Technology (NTNU), Trondheim, Norway., Kodama M; Center for Evolutionary Hologenomics, Globe Institute, Faculty of Health and Medical Sciences,University of Copenhagen, Copenhagen, Denmark., Rasmussen JA; Center for Evolutionary Hologenomics, Globe Institute, Faculty of Health and Medical Sciences,University of Copenhagen, Copenhagen, Denmark.; Department of Biology, Laboratory of Genomics and Molecular Biomedicine, University of Copenhagen, Copenhagen, Denmark., Hansen SB; Center for Evolutionary Hologenomics, Globe Institute, Faculty of Health and Medical Sciences,University of Copenhagen, Copenhagen, Denmark., Santos-Bay L; Center for Evolutionary Hologenomics, Globe Institute, Faculty of Health and Medical Sciences,University of Copenhagen, Copenhagen, Denmark., Lecaudey LA; Department of Natural History, NTNU University Museum, Norwegian University of Science and Technology (NTNU), Trondheim, Norway.; Aquaculture Department, SINTEF Ocean, Trondheim, Norway., Hansen M; Department of Environmental Science, Environmental Metabolomics Lab, Aarhus University, Roskilde, Denmark., Fjære E; Institute of Marine Research, Bergen, Norway., Myrmel LS; Institute of Marine Research, Bergen, Norway., Madsen L; Institute of Marine Research, Bergen, Norway.; Department of Clinical Medicine, University of Bergen, Norway, Bergen, Norway., Bernhard A; Institute of Marine Research, Bergen, Norway., Sveier H; Lerøy Seafood Group ASA, Bergen, Norway., Kristiansen K; Department of Biology, Laboratory of Genomics and Molecular Biomedicine, University of Copenhagen, Copenhagen, Denmark., Gilbert MTP; Department of Natural History, NTNU University Museum, Norwegian University of Science and Technology (NTNU), Trondheim, Norway.; Center for Evolutionary Hologenomics, Globe Institute, Faculty of Health and Medical Sciences,University of Copenhagen, Copenhagen, Denmark., Martin MD; Department of Natural History, NTNU University Museum, Norwegian University of Science and Technology (NTNU), Trondheim, Norway., Limborg MT; Center for Evolutionary Hologenomics, Globe Institute, Faculty of Health and Medical Sciences,University of Copenhagen, Copenhagen, Denmark.
Jazyk:	angličtina
Zdroj:	MSystems [mSystems] 2024 Feb 20; Vol. 9 (2), pp. e0104323. Date of Electronic Publication: 2024 Jan 31.
DOI:	10.1128/msystems.01043-23
Abstrakt:	Animals and their associated microbiota share long evolutionary histories. However, it is not always clear how host genotype and microbiota interact to affect phenotype. We applied a hologenomic approach to explore how host-microbiota interactions shape lifetime growth and parasite infection in farmed Atlantic salmon ( Salmo salar ). Multi-omics data sets were generated from the guts of 460 salmon, 82% of which were naturally infected with an intestinal cestode. A single Mycoplasma bacterial strain, MAG01, dominated the gut metagenome of large, non-parasitized fish, consistent with previous studies showing high levels of Mycoplasma in the gut microbiota of healthy salmon. While small and/or parasitized salmon also had high abundance of MAG01, we observed increased alpha diversity in these individuals, driven by increased frequency of low-abundance Vibrionaceae and other Mycoplasma species that carried known virulence genes. Colonization by one of these cestode-associated Mycoplasma strains was associated with host individual genomic variation in long non-coding RNAs. Integrating the multi-omic data sets revealed coordinated changes in the salmon gut mRNA transcriptome and metabolome that correlated with shifts in the microbiota of smaller, parasitized fish. Our results suggest that the gut microbiota of small and/or parasitized fish is in a state of dysbiosis that partly depends on the host genotype, highlighting the value of using a hologenomic approach to incorporate the microbiota into the study of host-parasite dynamics.IMPORTANCEStudying host-microbiota interactions through the perspective of the hologenome is gaining interest across all life sciences. Intestinal parasite infections are a huge burden on human and animal health; however, there are few studies investigating the role of the hologenome during parasite infections. We address this gap in the largest multi-omics fish microbiota study to date using natural cestode infection of farmed Atlantic salmon. We find a clear association between cestode infection, salmon lifetime growth, and perturbation of the salmon gut microbiota. Furthermore, we provide the first evidence that the genetic background of the host may partly determine how the gut microbiota changes during parasite-associated dysbiosis. Our study therefore highlights the value of a hologenomic approach for gaining a more in-depth understanding of parasitism. Competing Interests: H.S. is employed at Lerøy Seafood Group, who produces, markets, and sells farmed Atlantic salmon, including the fish used in the current investigation. Furthermore, Lerøy Seafood Group provided parts of the funding for this study. All other authors declare they have no competing interests.
Databáze:	MEDLINE
Externí odkaz:	Zobrazit plný text záznamu