Analysis of microbiota-host communication mediated by butyrate in Atlantic salmon
International audience Butyrate is a microbiota-produced metabolite, sensed by host short-chain fatty acid receptors FFAR2 (Gpr43), FFAR3 (Gpr41), HCAR2 (Gpr109A), and Histone deacetylase (HDAC) that promotes microbiota-host crosstalk. Butyrate influences energy uptake, developmental and immune resp...
Published in: | Computational and Structural Biotechnology Journal |
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Online Access: | https://hal.inrae.fr/hal-04297162 https://doi.org/10.1016/j.csbj.2023.03.050 |
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ftccsdartic:oai:HAL:hal-04297162v1 2024-02-27T08:38:46+00:00 Analysis of microbiota-host communication mediated by butyrate in Atlantic salmon Vargas, Rodrigo Soto-Aguilera, Sarita Parra, Mick Herrera, Sebastian Santibañez, Alvaro Kossack, Camila Saavedra, Claudia Mora, Oscar Pineda, Mauricio Gonzalez, Oscar Gonzalez, Alex Maisey, Kevin Torres-Maravilla, Edgar Bermúdez-Humarán, Luis Suárez-Villota, Elkin Tello, Mario Universidad de Santiago de Chile Santiago (USACH) Universidad Andrés Bello Santiago (UNAB) Centro Universitario de los Lagos - Universidad de Guadalajara (U de G) Universidad de Guadalajara-Nanotechnology laboratory Universidad Autónoma de Baja California (UABC) MICrobiologie de l'ALImentation au Service de la Santé (MICALIS) AgroParisTech-Université Paris-Saclay-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE) Universidad de Las Américas Ecuador (UDLA) 2023 https://hal.inrae.fr/hal-04297162 https://doi.org/10.1016/j.csbj.2023.03.050 en eng HAL CCSD Elsevier info:eu-repo/semantics/altIdentifier/doi/10.1016/j.csbj.2023.03.050 hal-04297162 https://hal.inrae.fr/hal-04297162 CERN: 37122632 doi:10.1016/j.csbj.2023.03.050 PUBMEDCENTRAL: PMC10130356 WOS: 000982616500001 http://creativecommons.org/licenses/by/ ISSN: 2001-0370 Computational and Structural Biotechnology Journal https://hal.inrae.fr/hal-04297162 Computational and Structural Biotechnology Journal, 2023, 21, pp.2558-2578. ⟨10.1016/j.csbj.2023.03.050⟩ Microbiota Butyrate Atlantic salmon [SDV.BBM]Life Sciences [q-bio]/Biochemistry Molecular Biology info:eu-repo/semantics/article Journal articles 2023 ftccsdartic https://doi.org/10.1016/j.csbj.2023.03.050 2024-01-28T00:20:54Z International audience Butyrate is a microbiota-produced metabolite, sensed by host short-chain fatty acid receptors FFAR2 (Gpr43), FFAR3 (Gpr41), HCAR2 (Gpr109A), and Histone deacetylase (HDAC) that promotes microbiota-host crosstalk. Butyrate influences energy uptake, developmental and immune response in mammals. This microbial metabolite is produced by around 79 anaerobic genera present in the mammalian gut, yet little is known about the role of butyrate in the host-microbiota interaction in salmonid fish. To further our knowledge of this interaction, we analyzed the intestinal microbiota and genome of Atlantic salmon (Salmo salar), searching for butyrate-producing genera and host butyrate receptors. We identified Firmicutes, Proteobacteria, and Actinobacteria as the main butyrate-producing bacteria in the salmon gut microbiota. In the Atlantic salmon genome, we identified an expansion of genes orthologous to FFAR2 and HCAR2 receptors, and class I and IIa HDACs that are sensitive to butyrate. In addition, we determined the expression levels of orthologous of HCAR2 in the gut, spleen, and head-kidney, and FFAR2 in RTgutGC cells. The effect of butyrate on the Atlantic salmon immune response was evaluated by analyzing the pro and anti-inflammatory cytokines response in vitro in SHK-1 cells by RT-qPCR. Butyrate decreased the expression of the pro-inflammatory cytokine IL-1 beta and increased anti-inflammatory IL-10 and TGF-beta cytokines. Butyrate also reduced the expression of interferon-alpha, Mx, and PKR, and decreased the viral load at a higher concentration (4 mM) in cells treated with this molecule before the infection with Infectious Pancreatic Necrosis Virus (IPNV) by mechanisms independent of FFAR2, FFAR3 and HCAR2 expression that probably inhibit HDAC. Moreover, butyrate modified phosphorylation of cytoplasmic proteins in RTgutGC cells. Our data allow us to infer that Atlantic salmon have the ability to sense butyrate produced by their gut microbiota via different specific targets, through which ... Article in Journal/Newspaper Atlantic salmon Salmo salar Archive ouverte HAL (Hyper Article en Ligne, CCSD - Centre pour la Communication Scientifique Directe) Computational and Structural Biotechnology Journal 21 2558 2578 |
institution |
Open Polar |
collection |
Archive ouverte HAL (Hyper Article en Ligne, CCSD - Centre pour la Communication Scientifique Directe) |
op_collection_id |
ftccsdartic |
language |
English |
topic |
Microbiota Butyrate Atlantic salmon [SDV.BBM]Life Sciences [q-bio]/Biochemistry Molecular Biology |
spellingShingle |
Microbiota Butyrate Atlantic salmon [SDV.BBM]Life Sciences [q-bio]/Biochemistry Molecular Biology Vargas, Rodrigo Soto-Aguilera, Sarita Parra, Mick Herrera, Sebastian Santibañez, Alvaro Kossack, Camila Saavedra, Claudia Mora, Oscar Pineda, Mauricio Gonzalez, Oscar Gonzalez, Alex Maisey, Kevin Torres-Maravilla, Edgar Bermúdez-Humarán, Luis Suárez-Villota, Elkin Tello, Mario Analysis of microbiota-host communication mediated by butyrate in Atlantic salmon |
topic_facet |
Microbiota Butyrate Atlantic salmon [SDV.BBM]Life Sciences [q-bio]/Biochemistry Molecular Biology |
description |
International audience Butyrate is a microbiota-produced metabolite, sensed by host short-chain fatty acid receptors FFAR2 (Gpr43), FFAR3 (Gpr41), HCAR2 (Gpr109A), and Histone deacetylase (HDAC) that promotes microbiota-host crosstalk. Butyrate influences energy uptake, developmental and immune response in mammals. This microbial metabolite is produced by around 79 anaerobic genera present in the mammalian gut, yet little is known about the role of butyrate in the host-microbiota interaction in salmonid fish. To further our knowledge of this interaction, we analyzed the intestinal microbiota and genome of Atlantic salmon (Salmo salar), searching for butyrate-producing genera and host butyrate receptors. We identified Firmicutes, Proteobacteria, and Actinobacteria as the main butyrate-producing bacteria in the salmon gut microbiota. In the Atlantic salmon genome, we identified an expansion of genes orthologous to FFAR2 and HCAR2 receptors, and class I and IIa HDACs that are sensitive to butyrate. In addition, we determined the expression levels of orthologous of HCAR2 in the gut, spleen, and head-kidney, and FFAR2 in RTgutGC cells. The effect of butyrate on the Atlantic salmon immune response was evaluated by analyzing the pro and anti-inflammatory cytokines response in vitro in SHK-1 cells by RT-qPCR. Butyrate decreased the expression of the pro-inflammatory cytokine IL-1 beta and increased anti-inflammatory IL-10 and TGF-beta cytokines. Butyrate also reduced the expression of interferon-alpha, Mx, and PKR, and decreased the viral load at a higher concentration (4 mM) in cells treated with this molecule before the infection with Infectious Pancreatic Necrosis Virus (IPNV) by mechanisms independent of FFAR2, FFAR3 and HCAR2 expression that probably inhibit HDAC. Moreover, butyrate modified phosphorylation of cytoplasmic proteins in RTgutGC cells. Our data allow us to infer that Atlantic salmon have the ability to sense butyrate produced by their gut microbiota via different specific targets, through which ... |
author2 |
Universidad de Santiago de Chile Santiago (USACH) Universidad Andrés Bello Santiago (UNAB) Centro Universitario de los Lagos - Universidad de Guadalajara (U de G) Universidad de Guadalajara-Nanotechnology laboratory Universidad Autónoma de Baja California (UABC) MICrobiologie de l'ALImentation au Service de la Santé (MICALIS) AgroParisTech-Université Paris-Saclay-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE) Universidad de Las Américas Ecuador (UDLA) |
format |
Article in Journal/Newspaper |
author |
Vargas, Rodrigo Soto-Aguilera, Sarita Parra, Mick Herrera, Sebastian Santibañez, Alvaro Kossack, Camila Saavedra, Claudia Mora, Oscar Pineda, Mauricio Gonzalez, Oscar Gonzalez, Alex Maisey, Kevin Torres-Maravilla, Edgar Bermúdez-Humarán, Luis Suárez-Villota, Elkin Tello, Mario |
author_facet |
Vargas, Rodrigo Soto-Aguilera, Sarita Parra, Mick Herrera, Sebastian Santibañez, Alvaro Kossack, Camila Saavedra, Claudia Mora, Oscar Pineda, Mauricio Gonzalez, Oscar Gonzalez, Alex Maisey, Kevin Torres-Maravilla, Edgar Bermúdez-Humarán, Luis Suárez-Villota, Elkin Tello, Mario |
author_sort |
Vargas, Rodrigo |
title |
Analysis of microbiota-host communication mediated by butyrate in Atlantic salmon |
title_short |
Analysis of microbiota-host communication mediated by butyrate in Atlantic salmon |
title_full |
Analysis of microbiota-host communication mediated by butyrate in Atlantic salmon |
title_fullStr |
Analysis of microbiota-host communication mediated by butyrate in Atlantic salmon |
title_full_unstemmed |
Analysis of microbiota-host communication mediated by butyrate in Atlantic salmon |
title_sort |
analysis of microbiota-host communication mediated by butyrate in atlantic salmon |
publisher |
HAL CCSD |
publishDate |
2023 |
url |
https://hal.inrae.fr/hal-04297162 https://doi.org/10.1016/j.csbj.2023.03.050 |
genre |
Atlantic salmon Salmo salar |
genre_facet |
Atlantic salmon Salmo salar |
op_source |
ISSN: 2001-0370 Computational and Structural Biotechnology Journal https://hal.inrae.fr/hal-04297162 Computational and Structural Biotechnology Journal, 2023, 21, pp.2558-2578. ⟨10.1016/j.csbj.2023.03.050⟩ |
op_relation |
info:eu-repo/semantics/altIdentifier/doi/10.1016/j.csbj.2023.03.050 hal-04297162 https://hal.inrae.fr/hal-04297162 CERN: 37122632 doi:10.1016/j.csbj.2023.03.050 PUBMEDCENTRAL: PMC10130356 WOS: 000982616500001 |
op_rights |
http://creativecommons.org/licenses/by/ |
op_doi |
https://doi.org/10.1016/j.csbj.2023.03.050 |
container_title |
Computational and Structural Biotechnology Journal |
container_volume |
21 |
container_start_page |
2558 |
op_container_end_page |
2578 |
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1792045733731368960 |