Core gut microbiota in rabbit: opportunities to strengthen the intestinal barrier

Sylvie Combes

https://orcid.org/0000-0002-2945-4423

France

Génétique Physiologie et Systèmes d'Elevage image/svg+xml

GenPhySE, Université de Toulouse, INRAE

Laurent Cauquil

https://orcid.org/0000-0002-0384-8811

France

Génétique Physiologie et Systèmes d'Elevage image/svg+xml

GenPhySE, Université de Toulouse, INRAE

Mathilde Rumeau

https://orcid.org/0009-0004-8903-0966

France

Génétique Physiologie et Systèmes d'Elevage image/svg+xml

GenPhySE, Université de Toulouse, INRAE

Charlotte Paës

https://orcid.org/0009-0002-4099-513X

France

Génétique Physiologie et Systèmes d'Elevage image/svg+xml

GenPhySE, Université de Toulouse, INRAE

----

INP-Purpan

Géraldine Pascal

https://orcid.org/0000-0002-5250-6594

France

Génétique Physiologie et Systèmes d'Elevage image/svg+xml

GenPhySE, Université de Toulouse, INRAE

Cláudia M. Vicente

https://orcid.org/0000-0001-8205-6486

France

Génétique Physiologie et Systèmes d'Elevage image/svg+xml

GenPhySE, Université de Toulouse, INRAE

Martin Beaumont

https://orcid.org/0000-0002-1559-2067

France

Génétique Physiologie et Systèmes d'Elevage image/svg+xml

GenPhySE, Université de Toulouse, INRAE

Christelle Knudsen

https://orcid.org/0000-0002-9587-8179

France

Génétique Physiologie et Systèmes d'Elevage image/svg+xml

GenPhySE, Université de Toulouse, INRAE

|

Accepted: 2025-03-12

|

Published: 2025-06-30

DOI: https://doi.org/10.4995/wrs.2025.23465
Funding Data

Downloads

Keywords:

intestinal epithelium, immune system, feed transition, meta-analysis

Supporting agencies:

French National Research Agency: ANR-JCJC MetaboWean (ANR-21-CE20-0048), ANR-PRC HoloOLIGO (ANR-21-CE20-0045-01)

INRAE metaprogramme Holoflux

Abstract:

The symbiotic relationship between the intestinal microbiota and its host is crucial to the development and functioning of both partners. The microbiota plays a key role in the development and physiology of its host (nutrition, growth, health and cognition). In turn, the host shapes the microbiota, according to factors that are intrinsic or dependent on its environment. However, the definition of an optimal microbiota that maximises ecosystem services (host benefits) has yet not been established. The symbiotic relationship between the microbiota and its host is based on a complex molecular dialogue at the level of the intestinal epithelium and the underlying mucosal immune system. These interactions condition the establishment of an intestinal barrier, limiting colonisation by microbial pathogens and thereby guaranteeing health. In this review, we propose a ‘core’ rabbit microbiota definition through a re-analysis of available opensource data. Based on the association between the abundance of bacterial taxa and host traits, we attempt to identify microbiota key species that would likely be involved in growth performance and health. Then, we describe the components of the intestinal barrier and the host-microbiota interaction mechanisms. Finally, we propose early in life nutritional levers to strengthen this intestinal barrier and thereby enhance the health of young rabbits before weaning.

Show more Show less

References:

Abecia L., Fondevila M., Balcells J., McEwan N.R. 2007. The effect of lactating rabbit does on the development of the caecal microbial community in the pups they nurture. J. Appl. Microbiol., 103: 557-564. https://doi.org/10.1111/j.1365-2672.2007.03277.x

Al Nabhani Z., Dulauroy S., Marques R., Cousu C., Al Bounny S., Déjardin F., Sparwasser T., Bérard M., Cerf-Bensussan N., Eberl G. 2019. A weaning reaction to microbiota is required for resistance to immunopathologies in the adult. Immunity, 50: 1276-1288.e5. https://doi.org/10.1016/j.immuni.2019.02.014

Allaoua M., Bonnafé E., Etienne P., Noirot V., Gabarrou J.-F., Castinel A., Pascal G., Darbot V., Treilhou M., Combes S. 2022. A carvacrol-based product reduces Campylobacter jejuni load and alters microbiota composition in the caeca of chickens. J. Appl. Microbiol., 132: 4501-4516. https://doi.org/10.1111/jam.15521

Andrani M., Borghetti P., Ravanetti F., Cavalli V., Ferrari L., De Angelis E., Martelli P., Saleri R. 2023. Acetate and propionate effects in response to LPS in a porcine intestinal co-culture model. Porc Health Manag, 9: 23. https://doi.org/10.1186/s40813-023-00316-y

Arrazuria R., Pérez V., Molina E., Juste R.A., Khafipour E., Elguezabal N. 2018. Diet induced changes in the microbiota and cell composition of rabbit gut associated lymphoid tissue (GALT). Sci Rep, 8: 14103. https://doi.org/10.1038/s41598-018-32484-1

Arumugam M., Raes J., Pelletier E., Le Paslier D., Yamada T., Mende D.R., Fernandes G.R., Tap J., Bruls T., Batto J.-M., Bertalan M., Borruel N., Casellas F., Fernandez L., Gautier L., Hansen T., Hattori M., Hayashi T., Kleerebezem M., Kurokawa K., Leclerc M., Levenez F., Manichanh C., Nielsen H.B., Nielsen T., Pons N., Poulain J., Qin J., Sicheritz-Ponten T., Tims S., Torrents D., Ugarte E., Zoetendal E.G., Wang J., Guarner F., Pedersen O., de Vos W.M., Brunak S., Dore J., Weissenbach J., Ehrlich S.D., Bork P. 2011. Enterotypes of the human gut microbiome. Nature, 473: 174-180. https://doi.org/10.1038/nature09944

Ayechu-Muruzabal V., van Stigt A.H., Mank M., Willemsen L.E.M., Stahl B., Garssen J., van’T Land B. 2018. Diversity of human milk oligosaccharides and effects on early life immune development. Front. Pediatr., 6: 239. https://doi.org/10.3389/fped.2018.00239

Baüerl C., Collado M.C., Zuniga M., Blas E., Martinez G.P. 2014. Changes in cecal microbiota and mucosal gene expression revealed new aspects of epizootic rabbit enteropathy. PLoS One, 9: e105707. https://doi.org/10.1371/journal.pone.0105707

Beaumont M., Paës C., Mussard E., Knudsen C., Cauquil L., Aymard P., Barilly C., Gabinaud B., Zemb O., Fourre S., Gautier R., Lencina C., Eutamène H., Theodorou V., Canlet C., Combes S. 2020. Gut microbiota derived metabolites contribute to intestinal barrier maturation at the suckling-to-weaning transition. Gut microbes, 11: 1268-1286. https://doi.org/10.1080/19490976.2020.1747335

Beaumont M., Mussard E., Barilly C., Lencina C., Gress L., Painteaux L., Gabinaud B., Cauquil L., Aymard P., Canlet C., Paës C., Knudsen C., Combes S. 2022. Developmental stage, solid food introduction, and suckling cessation differentially influence the comaturation of the gut microbiota and intestinal epithelium in rabbits. J Nutr, 152: 723-736. https://doi.org/10.1093/jn/nxab411

Belkaid Y., Harrison O.J. 2017. Homeostatic Immunity and the Microbiota. Immunity, 46: 562-576. https://doi.org/10.1016/j.immuni.2017.04.008

Birchenough G.M.H., Johansson M.E., Gustafsson J.K., Bergström J.H., Hansson G.C. 2015. New developments in goblet cell mucus secretion and function. Mucosal Immunol, 8: 712-719. https://doi.org/10.1038/mi.2015.32

Boll E.J., Lopez D.V., Terne M., Hessing S., Parschat K., Jensen S.R. 2024. Human milk oligosaccharides differentially support gut barrier integrity and enhance Th1 and Th17 cell effector responses in vitro. Front. Immunol., 15: 1359499. https://doi.org/10.3389/fimmu.2024.1359499

Carabaño R., Piquer J., Menoyo D., Badiola I. 2010. The digestive system of the rabbit, in: De Blas C., Wiseman J. (Eds.), Nutrition of the Rabbit. CABI, Wallingford, UK, pp. 1-18.

Caselli M., Holton J., Boldrini P., Vaira D., Calò G. 2010. Morphology of segmented filamentous bacteria and their patterns of contact with the follicle-associated epithelium of the mouse terminal ileum: Implications for the relationship with the immune system. Gut Microbes, 1: 367-372. https://doi.org/10.4161/gmic.1.6.14390

Casto-Rebollo C., Argente M.J., García M.L., Pena R.N., Blasco A., Ibáñez-Escriche N. 2023. Selection for environmental variance shifted the gut microbiome composition driving animal resilience. Microbiome, 11: 147. https://doi.org/10.1186/s40168-023-01580-4

Cauquil L., Beaumont M., Schmaltz-Panneau B., Liaubet L., Lippi Y., Naylies C., Bluy L., Poli M., Gress L., Lencina C., Duranthon V., Combes S. 2024. Coprophagia in early life tunes expression of immune genes after weaning in rabbit ileum. Sci Rep, 14: 8898. https://doi.org/10.1038/s41598-024-59591-6

Cesari V., Toschi I., Ferrazzi V., Cesari N., Grilli G., Lavazza A. 2009. Effect of weaning age and diet on growth performance, caecal characteristics and potential pathogenetic microflora in rabbits. World Rabbit Sci, 17: 195-205. https://doi.org/10.4995/wrs.2009.644

Chen C., Zibiao H., Ming Z., Shiyi C., Ruixia L., Jie W., SongJia L. 2014. Expression pattern of Toll-like receptors (TLRs) in different organs and effects of lipopolysaccharide on the expression of TLR 2 and 4 in reproductive organs of female rabbit. Dev Comp Immunol, 46: 341-348. https://doi.org/10.1016/j.dci.2014.05.008

Chen S.Y., Deng F., Jia X., Liu H., Zhang G.-W., Lai S.J. 2019. Gut microbiota profiling with differential tolerance against the reduced dietary fiber level in rabbit. Sci Rep, 9: 288. https://doi.org/10.1038/s41598-018-36534-6

Choudhury R., Middelkoop A., Boekhorst J., Gerrits W.J.J., Kemp B., Bolhuis J.E., Kleerebezem M. 2021. Early life feeding accelerates gut microbiome maturation and suppresses acute post-weaning stress in piglets. Environ Microbiol, 23: 7201-7213. https://doi.org/10.1111/1462-2920.15791

Combes S., Michelland R.J., Monteils V., Cauquil L., Soulie V., Tran N.U., Gidenne T., Fortun-Lamothe L. 2011. Postnatal development of the rabbit caecal microbiota composition and activity. FEMS Microbiol Ecol, 77: 680-689. https://doi.org/10.1111/j.1574-6941.2011.01148.x

Combes S., Fortun-Lamothe L., Cauquil L., Gidenne T. 2013. Engineering the rabbit digestive ecosystem to improve digestive health and efficacy. Animal, 7: 1429-1439. https://doi.org/10.1017/s1751731113001079

Combes S., Gidenne T., Cauquil L., Bouchez O., Fortun-Lamothe L. 2014. Coprophagous behavior of rabbit pups affects implantation of cecal microbiota and health status. J. Anim. Sci., 92: 652-665. https://doi.org/10.2527/jas.2013-6394

Combes S., Helies V., Lille-Laroucau C., Ruesche J., Poli M., Rumeau M., Beaumont M., Knudsen C., Venot E., Cholet S., Fenaille F. 2023. Variabilité de la composition en oligosaccharides du lait et lien avec la carrière reproductive des lapines et la viabilité des lapereaux au sevrage. Presented at the 19ème Journées de la Recherche Cunicole, Le Mans, France, pp. 86-90.

Comstock L.E., Kasper D.L. 2006. Bacterial glycans: key mediators of diverse host immune responses. Cell, 126: 847-850. https://doi.org/10.1016/j.cell.2006.08.021

Cotozzolo E., Cremonesi P., Curone G., Menchetti L., Riva F., Biscarini F., Marongiu M.L., Castrica M., Castiglioni B., Miraglia D., Luridiana S., Brecchia G. 2020. Characterization of bacterial microbiota composition along the gastrointestinal tract in rabbits. Animals, 11: 31. https://doi.org/10.3390/ani11010031

Cui C., Li L., Wu L., Wang X., Zheng Y., Wang F., Wei H., Peng J. 2023. Paneth cells in farm animals: current status and future direction. J Animal Sci Biotechnol, 14: 118. https://doi.org/10.1186/s40104-023-00905-5

Curone G., Biscarini F., Cotozzolo E., Menchetti L., Dal Bosco A., Riva F., Cremonesi P., Agradi S., Mattioli S., Castiglioni B., Di Giancamillo A., Cartoni Mancinelli A., Draghi S., Quattrone A., Collodel G., Modina S.C., Castellini C., Brecchia G. 2022. Could dietary supplementation with different sources of, N-3 polyunsaturated fatty acids modify the rabbit gut microbiota? Antibiotics, 11: 227. https://doi.org/10.3390/antibiotics11020227

De Vos W.M., Tilg H., van Hul M., Cani P.D. 2022. Gut microbiome and health: mechanistic insights. Gut, 71: 1020-1032. https://doi.org/10.1136/gutjnl-2021-326789

Drouet-Viard F., Fortun-Lamothe L. 2010. Review: I -The organisation and functioning of the immune system: particular features of the rabbit. World Rabbit Sci., 10: 15-23. https://doi.org/10.4995/wrs.2002.472

Du Y., Tu Y., Zhou Z., Hong R., Yan J., Zhang G.W. 2023. Effects of organic and inorganic copper on cecal microbiota and short-chain fatty acids in growing rabbits. Front. Vet. Sci., 10: 1179374. https://doi.org/10.3389/fvets.2023.1179374

Eisenhofer R., Nesme J., Santos-Bay L., Koziol A., Sørensen S.J., Alberdi A., Aizpurua O. 2024. A comparison of short-read, HiFi long-read, and hybrid strategies for genome-resolved metagenomics. Microbiol Spectr, 12: e03590-23. https://doi.org/10.1128/spectrum.03590-23

Escudié F., Auer L., Bernard M., Mariadassou M., Cauquil L., Vidal K., Maman S., Hernandez-Raquet G., Combes S., Pascal G. 2018. FROGS: Find, Rapidly, OTUs with Galaxy Solution. Bioinformatics, 34: 1287-1294. https://doi.org/10.1093/bioinformatics/btx791

Fang S., Chen X., Zhou L., Wang C., Chen Q., Lin R., Xiao T., Gan Q. 2019. Faecal microbiota and functional capacity associated with weaning weight in meat rabbits. Microb. Biotechnol., 12: 1441-1452. https://doi.org/10.1111/1751-7915.13485

Fortun-Lamothe L., Boullier S. 2007. A review on the interactions between gut microflora and digestive mucosal immunity. Possible ways to improve the health of rabbits. Livest. Sci., 107: 1-18. https://doi.org/10.1016/j.livsci.2006.09.005

Gallois M., Le Huërou-Luron I., Fortun-Lamothe L., Lallès J.P., Gidenne T. 2008. Adaptability of the digestive function according to age at weaning in the rabbit: I. Effect on feed intake and digestive functionality. Animal, 2: 525-535. https://doi.org/10.1017/S1751731108001729

García J., Gidenne T., Falçao-e-Cunha L., de Blas C. 2002. Identification of the main factors that influence caecal fermentation traits in growing rabbits. Anim. Res., 51: 165-173. https://doi.org/10.1051/animres:2002011

Ghosh S., Whitley C.S., Haribabu B., Jala V.R. 2021. Regulation of intestinal barrier function by microbial metabolites. Cell. Mol. Gastroenterol. Hepatol., 11: 1463-1482. https://doi.org/10.1016/j.jcmgh.2021.02.007

Gómez-Conde M.S., De Rozas A.P., Badiola I., Pérez-Alba L., De Blas C., Carabaño R., García J. 2009. Effect of neutral detergent soluble fibre on digestion, intestinal microbiota and performance in twenty five day old weaned rabbits. Livest. Sci., 125: 192-198. https://doi.org/10.1016/j.livsci.2009.04.010

Grant T.D., Specian R.D. 2001. Epithelial cell dynamics in rabbit cecum and proximal colon P1. Anat. Rec., 264: 427-437. https://doi.org/10.1002/ar.1161

Grimm P., Combes S., Pascal G., Cauquil L., Julliand V. 2019. Dietary composition and yeast/microalgae combination supplementation modulate the microbial ecosystem in the caecum, colon and faeces of horses. Brit. J. Nutr., 1-27. https://doi.org/10.1017/S0007114519002824

Gutiérrez I., Espinosa A., García J., Carabaño R., De Blas J.C. 2002. Effect of levels of starch, fiber, and lactose on digestion and growth performance of early-weaned rabbits. J. Anim. Sci., 80: 1029-1037. https://doi.org/10.2527/2002.8041029x

Heczko U., Abe A., Finlay B.B. 2000. Segmented filamentous bacteria prevent colonization of enteropathogenic Escherichia coli O103 in rabbits. J. Infect. Dis., 181: 1027-33. https://doi.org/10.1086/315348

Hertli S., Zimmermann P. 2022. Molecular interactions between the intestinal microbiota and the host. Mol. Microbiol., 117: 1297-1307. https://doi.org/10.1111/mmi.14905

Hosseinkhani F., Heinken A., Thiele I., Lindenburg P.W., Harms A.C., Hankemeier T. 2021. The contribution of gut bacterial metabolites in the human immune signaling pathway of noncommunicable diseases. Gut Microbes, 13: 1882927. https://doi.org/10.1080/19490976.2021.1882927

Hu X., Wang F., Yang S., Yuan X., Yang T., Zhou Y., Li Y. 2021. Rabbit microbiota across the whole body revealed by 16S rRNA gene amplicon sequencing. BMC Microbiol., 21: 312. https://doi.org/10.1186/s12866-021-02377-x

Hudson D., Distel H. 1982. The pattern of behaviour of rabbit pups in the nest. Behaviour, 79: 255-271. https://doi.org/10.1163/156853982X00292

Jin D.X., Zou H.W., Liu S.Q., Wang L.Z., Xue B., Wu D., Tian G., Cai J., Yan T.H., Wang Z.S., Peng Q.H. 2018. The underlying microbial mechanism of epizootic rabbit enteropathy triggered by a low fiber diet. Sci. Rep., 8: 12489. https://doi.org/10.1038/s41598-018-30178-2

Kacsala L., Szendrő Z., Gerencser Z., Radnai I., Kovacs M., Kasza R., Nagy I., Odermatt M., Atkari T., Matics Z. 2018. Early solid additional feeding of suckling rabbits from 3 to 15 days of age. Animal, 12: 28-33. https://doi.org/10.1017/s1751731117001367

Kardia E., Frese M., Smertina E., Strive T., Zeng X.-L., Estes M., Hall R.N. 2021. Culture and differentiation of rabbit intestinal organoids and organoid-derived cell monolayers. Sci Rep, 11:5401. https://doi.org/10.1038/s41598-021-84774-w

Kasbo J., Saleem M., Perwaiz S., Mignault D., Lamireau T., Tuchweber B., Yousef I. 2002. Biliary, fecal and plasma deoxycholic acid in rabbit, hamster, guinea pig, and rat: comparative study and implication in colon cancer. Biol. Pharm. Bull., 25: 1381-1384. https://doi.org/10.1248/bpb.25.1381

Kim J., Park W. 2015. Indole: a signaling molecule or a mere metabolic byproduct that alters bacterial physiology at a high concentration? J. Microbiol., 53: 421-428. https://doi.org/10.1007/s12275-015-5273-3

Knudsen C., Martins F., Cabau C., Zakaroff-Girard A., Riant E., Gallo L., Aymard P., Combes S., Beaumont M. 2022. Single cell RNA-sequencing, a tool to study the diversity of the lamina propria CD45+ cells in the rabbit caecum, in: 20th International Congress of Mucosal Immunology (ICMI2022). Presented at the 20th International Congress of Mucosal Immunology (ICMI2022), Seattle, United States.

Kong C., Elderman M., Cheng L., De Haan B.J., Nauta A., De Vos P. 2019. Modulation of intestinal epithelial glycocalyx development by human milk oligosaccharides and non‐digestible carbohydrates. Mol. Nutr. Food Res., 63: 1900303. https://doi.org/10.1002/mnfr.201900303

Kovács M., Szendrő Zs., Milisits G., Biro-Nemeth E., Radnai I., Posa R., Bónai A., Kovács F., Horn P. 2006. Effect of nursing method and faeces consumption on the development of bacteroides, lactobacillus and coliform flora in the caecum of the newborn rabbits. Reprod. Nut. Dev., 46: 205-210. https://doi.org/10.1051/rnd:2006010

Kovács M., Bónai A., Szendrő Z., Milisits G., Lukács H., Szabó- Fodor J., Tornyos G., Matics Z., Kovács F., Horn P. 2012. Effect of different weaning ages (21, 28 or 35 days) on production, growth and certain parameters of the digestive tract in rabbits. Animal, 6: 894-901. https://doi.org/10.1017/S1751731111002254

Kundu P., Blacher E., Elinav E., Pettersson S. 2017. Our gut microbiome: the evolving inner self. Cell, 171: 1481-1493. https://doi.org/10.1016/j.cell.2017.11.024

Lelouard H., Sahuquet A., Reggio H., Montcourrier P. 2001. Rabbit, M cells and dome enterocytes are distinct cell lineages. J. Cell Sci., 114: 2077-2083. https://doi.org/10.1242/jcs.114.11.2077

Lengliz S., Abbassi M.S., Rehaiem A., Ben Chehida N., Najar T. 2021. Characterization of bacteriocinogenic Enterococcus isolates from wild and laboratory rabbits for the selection of autochthonous probiotic strains in Tunisia. J. Appl. Microbiol., 131: 1474-1486. https://doi.org/10.1111/jam.15047

Ley R.E., Hamady M., Lozupone C., Turnbaugh P.J., Ramey R.R., Bircher J.S., Schlegel M.L., Tucker T.A., Schrenzel M.D., Knight R., Gordon J.I. 2008. Evolution of mammals and their gut microbes. Science, 320: 1647-1651. https://doi.org/10.1126/science.1155725

Li K., Pang S., Li Z., Ding X., Gan Y., Gan Q., Fang S. 2023. House ammonia exposure causes alterations in microbiota, transcriptome, and metabolome of rabbits. Front. Microbiol., 14: 1125195. https://doi.org/10.3389/fmicb.2023.1125195

Li S., Liu T., Wang K., Li C., Wu F., Yang X., Zhao M., Chen B., Chen X. 2023. The ratios of dietary non-fibrous carbohydrate (NFC) to neutral detergent fiber (NDF) influence intestinal immunity of rabbits by regulating gut microbiota composition and metabolites. Front. Microbiol., 14: 1146787. https://doi.org/10.3389/fmicb.2023.1146787

Li Z., He H., Ni M., Wang Z., Guo C., Niu Y., Xing S., Song M., Wang Y., Jiang Y., Yu L., Li M., Xu H. 2022. Microbiome-metabolome analysis of the immune microenvironment of the cecal contents, soft feces, and hard feces of hyplus rabbits. Oxid. Med. Cell Longev., 2022: 1-16. https://doi.org/10.1155/2022/5725442

Liu B., Cui Y., Ali Q., Zhu X., Li D., Ma S., Wang Z., Wang C., Shi Y. 2022. Gut microbiota modulate rabbit meat quality in response to dietary fiber. Front. Nutr., 9: 849429. https://doi.org/10.3389/fnut.2022.849429

Luo R., Zhang J., Zhang X., Zhou Z., Zhang W., Zhu Z., Liu H., Wang L., Zhong Z., Fu H., Jing B., Peng G. 2020. Bacillus subtilis HH2 ameliorates TNBS-induced colitis by modulating gut microbiota composition and improving intestinal barrier function in rabbit model. J. Funct. Foods, 74: 104167. https://doi.org/10.1016/j.jff.2020.104167

Ma L., Luo Z., Huang Y., Li Y., Guan J., Zhou T., Du Z., Yong K., Yao X., Shen L., Yu S., Zhong Z., Hu Y., Peng G., Shi X., Cao S. 2022. Modulating gut microbiota and metabolites with dietary fiber oat β-glucan interventions to improve growth performance and intestinal function in weaned rabbits. Front. Microbiol., 13: 1074036. https://doi.org/10.3389/fmicb.2022.1074036

Mach N., Berri M., Estellé J., Levenez F., Lemonnier G., Denis C., Leplat J.-J., Chevaleyre C., Billon Y., Doré J., Rogel-Gaillard C., Lepage P. 2015. Early-life establishment of the swine gut microbiome and impact on host phenotypes. Environ. Microbiol., 7: 554-569. https://doi.org/10.1111/1758-2229.12285

Maertens L., Lebas F., Szendrö Z. 2006. Rabbit milk: a review of quantity, quality and non-dietary affecting factors. World Rabbit Sci., 14: 205-230. https://doi.org/10.4995/wrs.2006.565

Malonga T., Vialaneix N., Beaumont M. 2024. BEST4 + cells in the intestinal epithelium. Am. J. Physiol. Cell Physiol., 326: C1345-C1352. https://doi.org/10.1152/ajpcell.00042.2024

Marcobal A., Barboza M., Sonnenburg E.D., Pudlo N., Martens E.C., Desai P., Lebrilla C.B., Weimer B.C., Mills D.A., German J.B., Sonnenburg J.L. 2011. Bacteroides in the infant gut consume milk oligosaccharides via mucus-utilization pathways. Cell Host Microbe, 10: 507-514. https://doi.org/10.1016/j.chom.2011.10.007

Martin-Gallausiaux C., Marinelli L., Blottière H.M., Larraufie P., Lapaque N. 2021. SCFA: mechanisms and functional importance in the gut. Proc. Nutr. Soc., 80: 37-49. https://doi.org/10.1017/S0029665120006916

Mattioli S., Dal Bosco A., Combes S., Moscati L., Crotti S., Cartoni Mancinelli A., Cotozzolo E., Castellini C. 2019. Dehydrated alfalfa and fresh grass supply in young rabbits: effect on performance and caecal microbiota biodiversity. Animals, 9: 341. https://doi.org/10.3390/ani9060341

McKenney E.S., Kendall M.M. 2016. Microbiota and pathogen ‘pas de deux’: setting up and breaking down barriers to intestinal infection. Pathog. Dis., 74. https://doi.org/10.1093/femspd/ftw051

Mora M., Velasco-Galilea M., Sánchez J.P., Ramayo-Caldas Y., Piles M. 2022. Disentangling the causal relationship between rabbit growth and cecal microbiota through structural equation models. Genet. Sel. Evol., 54: 81. https://doi.org/10.1186/s12711-022-00770-2

Mussard E., Pouzet C., Helies V., Pascal G., Fourre S., Cherbuy C., Rubio A., Vergnolle N., Combes S., Beaumont M. 2020. Culture of rabbit caecum organoids by reconstituting the intestinal stem cell niche in vitro with pharmacological inhibitors or, L-WRN conditioned medium. Stem Cell Res., 48: 1-10. https://doi.org/10.1016/j.scr.2020.101980

Padilha M.T.S., Licois D., Gidenne T., Carré B. 1999. Caecal microflora and fermentation pattern in exclusively milk-fed young rabbits. Reprod. Nutr. Dev., 39: 223-230. https://doi.org/10.1051/rnd:19990207

Paës C., Fortun-Lamothe L., Coureaud G., Bébin K., Duperray J., Gohier C., Guené-Grand E., Rebours G., Aymard P., Bannelier C., Debrusse A., Gidenne T., Combes S. 2020a. Insights into suckling rabbit feeding behaviour: acceptability of different creep feed presentations and attractiveness for sensory feed additives. Animal, 14: 1629-1637. https://doi.org/10.1017/s1751731120000038

Paës C., Gidenne T., Bébin K., Duperray J., Gohier C., Guené-Grand E., Rebours G., Bouchez O., Barilly C., Aymard P., Combes S. 2020b. Early introduction of solid feeds: ingestion level matters more than prebiotic supplementation for shaping gut microbiota. Front. Vet. Sci., 7. https://doi.org/10.3389/fvets.2020.00261

Paës C., Gidenne T., Bébin K., Duperray J., Gohier C., Guené-Grand E., Rebours G., Barilly C., Gabinaud B., Cauquil L., Castinel A., Pascal G., Darbot V., Aymard P., Debrusse A.-M., Beaumont M., Combes S. 2022. Early introduction of plant polysaccharides drives the establishment of rabbit gut bacterial ecosystems and the acquisition of microbial functions. mSystems, 18 p. https://doi.org/10.1128/msystems.00243-22

Pelaseyed T., Hansson G.C. 2020. Membrane mucins of the intestine at a glance. J. Cell Sci., 133: jcs240929. https://doi.org/10.1242/jcs.240929

Pereira F.C., Wasmund K., Cobankovic I., Jehmlich N., Herbold C.W., Lee K.S., Sziranyi B., Vesely C., Decker T., Stocker R., Warth B., Von Bergen M., Wagner M., Berry D. 2020. Rational design of a microbial consortium of mucosal sugar utilizers reduces Clostridiodes difficile colonization. Nat. Commun., 11: 5104. https://doi.org/10.1038/s41467-020-18928-1

Peterson L.W., Artis D. 2014. Intestinal epithelial cells: regulators of barrier function and immune homeostasis. Nat. Rev. Immunol., 14: 141-153. https://doi.org/10.1038/nri3608

Poretsky R., Rodriguez-R L.M., Luo C., Tsementzi D., Konstantinidis K.T. 2014. Strengths and limitations of 16S rRNA gene amplicon sequencing in revealing temporal microbial community dynamics. PLoS ONE, 9: e93827. https://doi.org/10.1371/journal.pone.0093827

Pott J., Hornef M. 2012. Innate immune signalling at the intestinal epithelium in homeostasis and disease. EMBO Rep, 13: 684-698. https://doi.org/10.1038/embor.2012.96

Puón-Peláez X.H.D., McEwan N.R., Álvarez-Martínez R.C., Mariscal-Landín G., Nava-Morales G.M., Mosqueda J., Olvera-Ramírez A.M. 2022. Effect of feeding insoluble fiber on the microbiota and metabolites of the caecum and feces of rabbits recovering from epizootic rabbit enteropathy relative to non-infected rabbits. Pathogens, 11: 571. https://doi.org/10.3390/pathogens11050571

Quast C., Pruesse E., Yilmaz P., Gerken J., Schweer T., Yarza P., Peplies J., Glöckner F.O. 2013. The SILVA ribosomal RNA gene database project: improved data processing and webbased tools. Nucleic Acids Res., 41: D590-D596. https://doi.org/10.1093/nar/gks1219

Rabbani G.H., John Albert M., Hamidur Rahman A.S.M., Moyenul Isalm M., Nasirul Islam K.M., Alam K. 1999. Short‐Chain Fatty Acids improve clinical, pathologic, and microbiologic features of experimental Shigellosis. J. Infect. Dis., 179: 390-397. https://doi.org/10.1086/314584

Read T., Fortun-Lamothe L., Pascal G., Le Boulch M., Cauquil L., Gabinaud B., Bannelier C., Balmisse E., Destombes N., Bouchez O., Gidenne T., Combes S. 2019. Diversity and cooccurrence pattern analysis of cecal microbiota establishment at the onset of solid feeding in young rabbits. Front. Microbiol., 10. https://doi.org/10.3389/fmicb.2019.00973

Rey M., Enjalbert F., Combes S., Cauquil L., Bouchez O., Monteils V. 2014. Establishment of ruminal bacterial community in dairy calves from birth to weaning is sequential. J. Appl. Microbiol., 116: 245-257. https://doi.org/10.1111/jam.12405

Rousseaux A., Brosseau C., Le Gall S., Piloquet H., Barbarot S., Bodinier M. 2021. Human milk oligosaccharides: their effects on the host and their potential as therapeutic agents. Front. Immunol., 12: 680911. https://doi.org/10.3389/fimmu.2021.680911

Satoh Y., Yamano M., Matsuda M., Ono K. 1990. Ultrastructure of Paneth cells in the intestine of various mammals. J. Elec. Microsc. Tech., 16: 69-80. https://doi.org/10.1002/jemt.1060160109

Savietto D., Paës C., Cauquil L., Fortun-Lamothe L., Combes S. 2020. Evolution of gut microbial community through reproductive life in female rabbits and investigation of the link with offspring survival. Animal, 14: 2253-2261. https://doi.org/10.1017/S1751731120001305

Scapinello C., Gidenne T., Fortun-Lamothe L. 1999. Digestive capacity of the rabbit during the post-weaning period, according to the milk/solid feed intake pattern before weaning. Reprod. Nutr. Dev., 39: 423-432. https://doi.org/10.1051/rnd:19990402

Sekirov I., Finlay B.B. 2009. The role of the intestinal microbiota in enteric infection. J. Physiol., 587: 4159-4167. https://doi.org/10.1113/jphysiol.2009.172742

Sepahi A., Liu Q., Friesen L., Kim C.H. 2021. Dietary fiber metabolites regulate innate lymphoid cell responses. Mucosal Immunol, 14: 317-330. https://doi.org/10.1038/s41385-020-0312-8

Silverman J.B., Vega P.N., Tyska M.J., Lau K.S. 2024. Intestinal Tuft Cells: Morphology, Function, and Implications for Human Health. Ann. Rev. Physiol., 86: 479-504. https://doi.org/10.1146/annurev-physiol-042022-030310

Simon P.M., Goode P.L., Mobasseri A., Zopf D. 1997. Inhibition of Helicobacter pylori binding to gastrointestinal epithelial cells by sialic acid-containing oligosaccharides. Infect Immun, 65:750-757. https://doi.org/10.1128/iai.65.2.750-757.1997

Simonová M., Lauková A. 2007. Bacteriocin activity of Enterococci from rabbits. Vet. Res. Commun., 31: 143-152. https://doi.org/10.1007/s11259-006-3411-4

Sonnenburg J.L., Bäckhed F. 2016. Diet-microbiota interactions as moderators of human metabolism. Nature, 535: 56-64. https://doi.org/10.1038/nature18846

Szeligowska N., Cholewińska P., Czyż K., Wojnarowski K., Janczak M. 2021. Inter and intraspecies comparison of the level of selected bacterial phyla in in cattle and sheep based on feces. BMC Vet. Res., 17: 224. https://doi.org/10.1186/s12917-021-02922-w

Tizard I.R. 2023. Comparative mammalian immunology: the evolution and diversity of the immune systems of mammals. Academic Press, Cambridge, MA.

Velasco-Galilea M., Piles M., Viñas M., Rafel O., González-Rodríguez O., Guivernau M., Sánchez J.P. 2018. Rabbit microbiota changes throughout the intestinal tract. Front. Microbiol., 9: 2144. https://doi.org/10.3389/fmicb.2018.02144

Velasco-Galilea M., Guivernau M., Piles M., Viñas M., Rafel O., Sánchez A., Ramayo-Caldas Y., González-Rodríguez O., Sánchez J.P. 2020. Breeding farm, level of feeding and presence of antibiotics in the feed influence rabbit cecal microbiota. Anim. Microbiome, 2: 40. https://doi.org/10.1186/s42523-020-00059-z

Velasco-Galilea M., Piles M., Ramayo-Caldas Y., Sánchez J.P. 2021. The value of gut microbiota to predict feed efficiency and growth of rabbits under different feeding regimes. Sci. Rep., 11: 19495. https://doi.org/10.1038/s41598-021-99028-y

Velasco-Galilea M., Piles M., Ramayo-Caldas Y., Varona L., Sánchez J.P. 2022. Use of Bayes factors to evaluate the effects of host genetics, litter and cage on the rabbit cecal microbiota. Genet. Sel. Evol., 54: 46. https://doi.org/10.1186/s12711-022-00738-2

Vidal J.E., Ma M., Saputo J., Garcia J., Uzal F.A., McClane B.A. 2012. Evidence that the Agr‐like quorum sensing system regulates the toxin production, cytotoxicity and pathogenicity of Clostridium perfringens type, C isolate CN3685. Mol. Microbiol., 83: 179-194. https://doi.org/10.1111/j.1365-2958.2011.07925.x

Viggiano D., Ianiro G., Vanella G., Bibbò S., Bruno G., Simeone G., Mele G. 2015. Gut barrier in health and disease: focus on childhood. Eur. Rev. Med. Pharmacol. Sci., 19: 1077-1085.

Wagner C., Torow N., Hornef M.W., Lelouard H. 2022. Spatial and temporal key steps in early‐life intestinal immune system development and education. FEBS J., 289: 4731-4757. https://doi.org/10.1111/febs.16047

Walsh C., Lane J.A., van Sinderen D., Hickey R.M. 2020. Human milk oligosaccharides: Shaping the infant gut microbiota and supporting health. J. Funct. Foods, 72: 104074. https://doi.org/10.1016/j.jff.2020.104074

Wang L., Tang L., Feng Y., Zhao S., Han M., Zhang C., Yuan G., Zhu J., Cao S., Wu Q., Li L., Zhang Z. 2020. A purified membrane protein from Akkermansia muciniphila or the pasteurised bacterium blunts colitis associated tumourigenesis by modulation of CD8 + T cells in mice. Gut, 69: 1988-1997. https://doi.org/10.1136/gutjnl-2019-320105

Wang Q.J., Guo Y., Zhang K.H., Zhang L., Geng S.X., Shan C.H., Liu P., Zhu M.-Q., Jin Q.Y., Liu Z.Y., Wang M.Z., Li M.Y., Liu M., An L., Tian J.H., Wu Z.H. 2021. Night-restricted feeding improves gut health by synchronizing microbe-driven serotonin rhythm and eating activity-driven body temperature oscillations in growing rabbits. Front. Cell. Infect. Microbiol., 11: 771088. https://doi.org/10.3389/fcimb.2021.771088

Wu D., Xia M., Yan A., Jiang H., Fan J., Zhou S., Wei X., Liu S., Chen B. 2023. Carvacrol attenuated lipopolysaccharide-induced intestinal injury by down-regulating TLRs gene expression and regulating the gut microbiota in rabbit. Sci Rep, 13: 11447. https://doi.org/10.1038/s41598-023-38577-w

Yang G., Zhao F., Tian H., Li J., Guo D. 2020. Effects of the dietary digestible fiber-to-starch ratio on pellet quality, growth and cecal microbiota of Angora rabbits. Asian-Australas. J. Anim. Sci., 33: 623-633. https://doi.org/10.5713/ajas.19.0221

Yatsunenko T., Rey F.E., Manary M.J., Trehan I., Dominguez-Bello M.G., Contreras M., Magris M., Hidalgo G., Baldassano R.N., Anokhin A.P., Heath A.C., Warner B., Reeder J., Kuczynski J., Caporaso J.G., Lozupone C.A., Lauber C., Clemente J.C., Knights D., Knight R., Gordon J.I. 2012. Human gut microbiome viewed across age and geography. Nature, 486: 222-227.

Ye D., Ding X., Pang S., Gan Y., Li Z., Gan Q., Fang S. 2023. Seasonal variations in production performance, health status, and gut microbiota of meat rabbit reared in semi-confined conditions. Animals, 14: 113. https://doi.org/10.3390/ani14010113

Ye X.X., Li K.Y., Li Y.F., Lu J.N., Guo P.T., Liu H.Y., Zhou L.W., Xue S.S., Huang C.Y., Fang S.M., Gan Q.F. 2022. The effects of Clostridium butyricum on Ira rabbit growth performance, cecal microbiota and plasma metabolome. Front. Microbiol., 13: 974337. https://doi.org/10.3390/fmicb.2022.974337

Yu Z.T., Nanthakumar N.N., Newburg D.S. 2016. The human milk oligosaccharide 2'-fucosyllactose quenches Campylobacter jejuni-induced inflammation in human epithelial cells HEp-2 and HT-29 and in mouse intestinal mucosa. J. Nutr., 146: 1980-1990. https://doi.org/10.3945/jn.116.230706

Zhao M., Liu H., Liu M., Yue Z., Li C., Liu L., Li F. 2024. Metagenomics and metabolomics reveal that gut microbiome adapts to the diet transition in Hyla rabbits. Microbiol. Res., 283: 127705. https://doi.org/10.1016/j.micres.2024.127705

Zhu C., Feng S., Sperandio V., Yang Z., Thate T.E., Kaper J.B., Boedeker E.C. 2007. The possible influence of LuxS in the in vivo virulence of rabbit enteropathogenic Escherichia coli. Vet. Microbiol., 125: 313-322. https://doi.org/10.1016/j.vetmic.2007.05.030

Zhu Y., Wang C., Li F. 2015. Impact of dietary fiber/starch ratio in shaping caecal microbiota in rabbits. Can. J. Microbiol., 61: 771-784. https://doi.org/10.1139/cjm-2015-0201

Show more Show less