Yanxian Li1, Leonardo Bruni2, Alexander Jaramillo-Torres3, Karina Gajardo3, Trond M Kortner3, Åshild Krogdahl3. 1. Department of Paraclinical Sciences, Faculty of Veterinary Medicine, Norwegian University of Life Sciences, Oslo, Norway. yanxian.li@nmbu.no. 2. Department of Agriculture, Food, Environment and Forestry, University of Florence, Florence, Italy. 3. Department of Paraclinical Sciences, Faculty of Veterinary Medicine, Norwegian University of Life Sciences, Oslo, Norway.
Abstract
BACKGROUND: Intestinal digesta is commonly used for studying responses of microbiota to dietary shifts, yet evidence is accumulating that it represents an incomplete view of the intestinal microbiota. The present work aims to investigate the differences between digesta- and mucosa-associated intestinal microbiota in Atlantic salmon (Salmo salar) and how they may respond differently to dietary perturbations. In a 16-week seawater feeding trial, Atlantic salmon were fed either a commercially-relevant reference diet or an insect meal diet containing ~ 15% black soldier fly (Hermetia illucens) larvae meal. The digesta- and mucosa-associated distal intestinal microbiota were profiled by 16S rRNA gene sequencing. RESULTS: Regardless of diet, we observed substantial differences between digesta- and mucosa-associated intestinal microbiota. Microbial richness and diversity were much higher in the digesta than the mucosa. The insect meal diet altered the distal intestinal microbiota resulting in higher microbial richness and diversity. The diet effect, however, depended on the sample origin. Digesta-associated intestinal microbiota showed more pronounced changes than the mucosa-associated microbiota. Multivariate association analyses identified two mucosa-enriched taxa, Brevinema andersonii and Spirochaetaceae, associated with the expression of genes related to immune responses and barrier function in the distal intestine, respectively. CONCLUSIONS: Our data show that salmon intestinal digesta and mucosa harbor microbial communities with clear differences. While feeding insects increased microbial richness and diversity in both digesta- and mucosa-associated intestinal microbiota, mucosa-associated intestinal microbiota seems more resilient to variations in the diet composition. To fully unveil the response of intestinal microbiota to dietary changes, concurrent profiling of digesta- and mucosa-associated intestinal microbiota is recommended whenever feasible. Specific taxa enriched in the intestinal mucosa are associated to gene expression related to immune responses and barrier function. Detailed studies are needed on the ecological and functional significance of taxa associated to intestinal microbiota dwelling on the mucosa.
BACKGROUND: Intestinal digesta is commonly used for studying responses of microbiota to dietary shifts, yet evidence is accumulating that it represents an incomplete view of the intestinal microbiota. The present work aims to investigate the differences between digesta- and mucosa-associated intestinal microbiota in Atlantic salmon (Salmo salar) and how they may respond differently to dietary perturbations. In a 16-week seawater feeding trial, Atlantic salmon were fed either a commercially-relevant reference diet or an insect meal diet containing ~ 15% black soldier fly (Hermetia illucens) larvae meal. The digesta- and mucosa-associated distal intestinal microbiota were profiled by 16S rRNA gene sequencing. RESULTS: Regardless of diet, we observed substantial differences between digesta- and mucosa-associated intestinal microbiota. Microbial richness and diversity were much higher in the digesta than the mucosa. The insect meal diet altered the distal intestinal microbiota resulting in higher microbial richness and diversity. The diet effect, however, depended on the sample origin. Digesta-associated intestinal microbiota showed more pronounced changes than the mucosa-associated microbiota. Multivariate association analyses identified two mucosa-enriched taxa, Brevinema andersonii and Spirochaetaceae, associated with the expression of genes related to immune responses and barrier function in the distal intestine, respectively. CONCLUSIONS: Our data show that salmon intestinal digesta and mucosa harbor microbial communities with clear differences. While feeding insects increased microbial richness and diversity in both digesta- and mucosa-associated intestinal microbiota, mucosa-associated intestinal microbiota seems more resilient to variations in the diet composition. To fully unveil the response of intestinal microbiota to dietary changes, concurrent profiling of digesta- and mucosa-associated intestinal microbiota is recommended whenever feasible. Specific taxa enriched in the intestinal mucosa are associated to gene expression related to immune responses and barrier function. Detailed studies are needed on the ecological and functional significance of taxa associated to intestinal microbiota dwelling on the mucosa.
Entities:
Keywords:
Atlantic salmon; Black soldier fly; Diet; Digesta; Microbiota; Mucosa
Authors: E Wynants; L Frooninckx; S Crauwels; C Verreth; J De Smet; C Sandrock; J Wohlfahrt; J Van Schelt; S Depraetere; B Lievens; S Van Miert; J Claes; L Van Campenhout Journal: Microb Ecol Date: 2018-11-14 Impact factor: 4.552
Authors: Carlotta De Filippo; Duccio Cavalieri; Monica Di Paola; Matteo Ramazzotti; Jean Baptiste Poullet; Sebastien Massart; Silvia Collini; Giuseppe Pieraccini; Paolo Lionetti Journal: Proc Natl Acad Sci U S A Date: 2010-08-02 Impact factor: 11.205
Authors: J Paul Brooks; David J Edwards; Michael D Harwich; Maria C Rivera; Jennifer M Fettweis; Myrna G Serrano; Robert A Reris; Nihar U Sheth; Bernice Huang; Philippe Girerd; Jerome F Strauss; Kimberly K Jefferson; Gregory A Buck Journal: BMC Microbiol Date: 2015-03-21 Impact factor: 3.605
Authors: Tamsyn M Uren Webster; Sofia Consuegra; Matthew Hitchings; Carlos Garcia de Leaniz Journal: Appl Environ Microbiol Date: 2018-08-01 Impact factor: 4.792
Authors: Andrew J Hryckowian; William Van Treuren; Samuel A Smits; Nicole M Davis; Jackson O Gardner; Donna M Bouley; Justin L Sonnenburg Journal: Nat Microbiol Date: 2018-04-23 Impact factor: 17.745
Authors: Ana Basto; Josep Calduch-Giner; Beatriz Oliveira; Lisa Petit; Tiago Sá; Margarida R G Maia; Susana C Fonseca; Elisabete Matos; Jaume Pérez-Sánchez; Luisa M P Valente Journal: Front Physiol Date: 2021-04-15 Impact factor: 4.566
Authors: Pabodha Weththasinghe; Sérgio D C Rocha; Ove Øyås; Leidy Lagos; Jon Ø Hansen; Liv T Mydland; Margareth Øverland Journal: Anim Microbiome Date: 2022-01-15
Authors: Fábio Rangel; Paula Enes; Laura Gasco; Francesco Gai; Bela Hausmann; David Berry; Aires Oliva-Teles; Claudia R Serra; Fátima C Pereira Journal: Front Microbiol Date: 2022-04-12 Impact factor: 6.064
Authors: Michael D Martin; Morten T Limborg; Jaelle C Brealey; Laurène A Lecaudey; Miyako Kodama; Jacob A Rasmussen; Harald Sveier; Nolwenn M Dheilly Journal: mBio Date: 2022-05-03 Impact factor: 7.786
Authors: Carlos Muñoz; Josue González-Lorca; Mick Parra; Sarita Soto; Natalia Valdes; Ana María Sandino; Rodrigo Vargas; Alex González; Mario Tello Journal: Front Immunol Date: 2021-08-12 Impact factor: 7.561