Transkingdom network analysis provides insight into host-microbiome interactions in Atlantic salmon

Background: The Atlantic salmon gut constitutes an intriguing system for studying host-microbiota interactions due to the dramatic environmental change salmon experiences during its life cycle. Yet, little is known about the role of interactions in this system and there is a general deficit in compu...

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Main Authors: Marius A. Strand, Yang Jin, Simen R. Sandve, Phil B. Pope, Torgeir R. Hvidsten
Format: Article
Language:English
Published: Elsevier 2021-01-01
Series:Computational and Structural Biotechnology Journal
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S2001037021000428
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spelling doaj-83adaa0fe4824cd5ab4d3c297e960a342021-02-09T04:06:22ZengElsevierComputational and Structural Biotechnology Journal2001-03702021-01-011910281034Transkingdom network analysis provides insight into host-microbiome interactions in Atlantic salmonMarius A. Strand0Yang Jin1Simen R. Sandve2Phil B. Pope3Torgeir R. Hvidsten4Faculty of Biosciences, Norwegian University of Life Sciences, 1432 Ås, Norway; Faculty of Chemistry, Biotechnology and Food Science, Norwegian University of Life Sciences, 1432 Ås, NorwayFaculty of Biosciences, Norwegian University of Life Sciences, 1432 Ås, NorwayFaculty of Biosciences, Norwegian University of Life Sciences, 1432 Ås, NorwayFaculty of Biosciences, Norwegian University of Life Sciences, 1432 Ås, Norway; Faculty of Chemistry, Biotechnology and Food Science, Norwegian University of Life Sciences, 1432 Ås, NorwayFaculty of Chemistry, Biotechnology and Food Science, Norwegian University of Life Sciences, 1432 Ås, Norway; Corresponding author at: Universitetstunet 3, 1433 Ås, Norway.Background: The Atlantic salmon gut constitutes an intriguing system for studying host-microbiota interactions due to the dramatic environmental change salmon experiences during its life cycle. Yet, little is known about the role of interactions in this system and there is a general deficit in computational methods for integrative analysis of omics data from host-microbiota systems. Methods: We developed a pipeline to integrate host RNAseq data and microbial 16S rRNA amplicon sequencing data using weighted correlation network analysis. Networks are first inferred from each dataset separately, followed by module detections and finally robust identification of interactions via comparisons of representative module profiles. Through the use of module profiles, this network-based dimensionality reduction approach provides a holistic view into the discovery of potential host-microbiota symbionts. Results: We analyzed host gene expression from the gut epithelial tissue and microbial abundances from the salmon gut in a long-term feeding trial spanning the fresh-/salt-water transition and including two feeds resembling the fatty acid compositions available in salt- and fresh-water environments, respectively. We identified several host modules with significant correlations to both microbiota modules and variables such as feed, growth and sex. Although the strongest associations largely coincided with the fresh-/salt-water transition, there was a second layer of correlations associating smaller host modules to both variables and microbiota modules. Hence, we identify extensive reprogramming of the gut epithelial transcriptome and large scale coordinated changes in gut microbiota composition associated with water type as well as evidence of host-microbiota interactions linked to feed.http://www.sciencedirect.com/science/article/pii/S2001037021000428Transkingdom network analysisHost-microbiome interactions
collection DOAJ
language English
format Article
sources DOAJ
author Marius A. Strand
Yang Jin
Simen R. Sandve
Phil B. Pope
Torgeir R. Hvidsten
spellingShingle Marius A. Strand
Yang Jin
Simen R. Sandve
Phil B. Pope
Torgeir R. Hvidsten
Transkingdom network analysis provides insight into host-microbiome interactions in Atlantic salmon
Computational and Structural Biotechnology Journal
Transkingdom network analysis
Host-microbiome interactions
author_facet Marius A. Strand
Yang Jin
Simen R. Sandve
Phil B. Pope
Torgeir R. Hvidsten
author_sort Marius A. Strand
title Transkingdom network analysis provides insight into host-microbiome interactions in Atlantic salmon
title_short Transkingdom network analysis provides insight into host-microbiome interactions in Atlantic salmon
title_full Transkingdom network analysis provides insight into host-microbiome interactions in Atlantic salmon
title_fullStr Transkingdom network analysis provides insight into host-microbiome interactions in Atlantic salmon
title_full_unstemmed Transkingdom network analysis provides insight into host-microbiome interactions in Atlantic salmon
title_sort transkingdom network analysis provides insight into host-microbiome interactions in atlantic salmon
publisher Elsevier
series Computational and Structural Biotechnology Journal
issn 2001-0370
publishDate 2021-01-01
description Background: The Atlantic salmon gut constitutes an intriguing system for studying host-microbiota interactions due to the dramatic environmental change salmon experiences during its life cycle. Yet, little is known about the role of interactions in this system and there is a general deficit in computational methods for integrative analysis of omics data from host-microbiota systems. Methods: We developed a pipeline to integrate host RNAseq data and microbial 16S rRNA amplicon sequencing data using weighted correlation network analysis. Networks are first inferred from each dataset separately, followed by module detections and finally robust identification of interactions via comparisons of representative module profiles. Through the use of module profiles, this network-based dimensionality reduction approach provides a holistic view into the discovery of potential host-microbiota symbionts. Results: We analyzed host gene expression from the gut epithelial tissue and microbial abundances from the salmon gut in a long-term feeding trial spanning the fresh-/salt-water transition and including two feeds resembling the fatty acid compositions available in salt- and fresh-water environments, respectively. We identified several host modules with significant correlations to both microbiota modules and variables such as feed, growth and sex. Although the strongest associations largely coincided with the fresh-/salt-water transition, there was a second layer of correlations associating smaller host modules to both variables and microbiota modules. Hence, we identify extensive reprogramming of the gut epithelial transcriptome and large scale coordinated changes in gut microbiota composition associated with water type as well as evidence of host-microbiota interactions linked to feed.
topic Transkingdom network analysis
Host-microbiome interactions
url http://www.sciencedirect.com/science/article/pii/S2001037021000428
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