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Evolution of gut microbial community through reproductive life in female rabbits and investigation of the link with offspring survival

Published online by Cambridge University Press:  18 June 2020

D. Savietto Open the ORCID record for D. Savietto [Opens in a new window] ,
C. Paës ,
L. Cauquil Open the ORCID record for L. Cauquil [Opens in a new window] ,
L. Fortun-Lamothe Open the ORCID record for L. Fortun-Lamothe [Opens in a new window]  and
S. Combes Open the ORCID record for S. Combes [Opens in a new window]
D. Savietto*
Affiliation:
GenPhySE, Université de Toulouse, INRAE, ENVT, F-31326Castanet-Tolosan, France
C. Paës
Affiliation:
GenPhySE, Université de Toulouse, INRAE, ENVT, F-31326Castanet-Tolosan, France
L. Cauquil
Affiliation:
GenPhySE, Université de Toulouse, INRAE, ENVT, F-31326Castanet-Tolosan, France
L. Fortun-Lamothe
Affiliation:
GenPhySE, Université de Toulouse, INRAE, ENVT, F-31326Castanet-Tolosan, France
S. Combes
Affiliation:
GenPhySE, Université de Toulouse, INRAE, ENVT, F-31326Castanet-Tolosan, France
*
†E-mail: davi.savietto@inrae.fr
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Abstract

The digestive microbiota plays a decisive role in shaping and preserving health throughout life. Rabbit younglings are born with a sterile digestive tract but then it gets progressively colonised by the microbiota of the nursing mother, by entering in contact with or ingesting the maternal droppings present in the nest. Here we posit that (i) offspring survival and (ii) lifespan of female rabbits are linked to how diverse their microbiota are. To test the hypothesis that maternal microbiota evolves in females having had different levels of offspring survival in their lifetime, we obtained 216 hard faecal samples from 75 female rabbits at ages 19.6, 31.6, 62.6 and 77.6 weeks. The annual mean offspring survival (MOS) at 64 days was calculated for each female then crossed against three alpha-diversity indexes (operational taxonomic units (OTUs), inverse Simpson index and Shannon index). Age was also analysed against these three parameters. The alpha-diversity indexes of the female faecal microbiota did not correlate with MOS, but they did decrease with age (e.g. from 712 OTUs at age 19.6 weeks to 444 OTUs at 77.6 weeks; P < 0.05). The age effect was also found in beta-diversity non-metric multidimensional scaling plots using the Bray–Curtis dissimilarity index and the unweighted UniFrac index but not for MOS. The ability of the microbiota composition from the faecal samples of young females (19.6 weeks old) to predict their lifespan was also evaluated. After subdividing the initial population into two classes (females that weaned a maximum of three litters and females living longer), we found no clear distinction between these two classes. To our knowledge, this is the first long-term study to characterise the gut microbiota of adult female rabbits through their reproductive life, thus laying foundations for using the gut microbiota data and its influence in studies on adult rabbits.

Keywords

Oryctolagus cuniculus16s rDNAdigestive microbiotaoffspring survivalfemale lifespan
Type
Research Article
Information
animal , Volume 14 , Issue 11 , November 2020 , pp. 2253 - 2261
Copyright
© The Author(s), 2020. Published by Cambridge University Press on behalf of The Animal Consortium

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References

Anderson, MJ 2001. A new method for non-parametric multivariate analysis of variance. Austral Ecology 26, 32–46.Google Scholar
Biagi, E, Nylund, L, Candela, M, Ostan, R, Bucci, L, Pini, E, Nikkïla, J, Monti, D, Satokari, R, Franceschi, C, Brigidi, P and Vos, WD 2010. Through ageing, and beyond: gut microbiota and inflammatory status in seniors and centenarians. PLoS ONE 5, e10667.Google ScholarPubMed
Combes, S, Gidenne, T, Cauquil, L, Bouchez, O and Fortun-Lamothe, L 2014. Coprophagous behavior of rabbit pups affects implantation of cecal microbiota and health status. Journal of Animal Science 92, 652–665.CrossRefGoogle ScholarPubMed
Combes, S, Massip, K, Martin, O, Furbeyre, H, Cauquil, L, Pascal, G, Bouchez, O, Le Floc’h, N, Zemb, O, Oswald, IP and Gidenne, T 2017. Impact of feed restriction and housing hygiene conditions on specific and inflammatory immune response, the cecal bacterial community and the survival of young rabbits. Animal 11, 854–863.CrossRefGoogle ScholarPubMed
Escudié, F, Auer, L, Bernard, M, Mariadassou, M, Cauquil, L, Vidal, K, Maman, S, Hernandez-Raquet, G, Combes, S and Pascal, G 2018. FROGS: find, rapidly, OTUs with galaxy solution. Bioinformatics 34, 1287–1294.CrossRefGoogle ScholarPubMed
Fernández-Carmona, J, Cervera, C and Blas, E 1996. Prediction of the energy value of rabbit feeds varying widely in fibre content. Animal Feed Science and Technology 64, 61–75.CrossRefGoogle Scholar
Fortun-Lamothe, L and Boullier, S 2007. A review on the interactions between gut microflora and digestive mucosal immunity. Possible ways to improve the health of rabbits. Livestock Science 107, 1–18.CrossRefGoogle Scholar
Gelain, M 2017. Rabbit dam’s influence in the offspring mortality. Master’s thesis, University of Padua, Padua, Italy.Google Scholar
Jašarević, E, Howard, CD, Misic, AM, Beiting, DP and Bale, TL 2017. Stress during pregnancy alters temporal and spatial dynamics of the maternal and offspring microbiome in a sex-specific manner. Scientific Reports 7, 44182.CrossRefGoogle Scholar
Kelly, D, King, T and Aminov, R 2007. Importance of microbial colonization of the gut in early life to the development of immunity. Mutation Research 622, 58–69.Google ScholarPubMed
Koleva, PT, Kim, JS, Scott, JA and Kozyrskyj, AL 2015. Microbial programming of health and disease starts during fetal life. Birth Defects Research, Part C. Embryo Today: Reviews 105, 265–277.Google ScholarPubMed
Mahé, F, Rognes, T, Quince, C, de Vargas, C and Dunthorn, M 2014. Swarm: robust and fast clustering method for amplicon-based studies. PeerJ 2, e593.CrossRefGoogle ScholarPubMed
McMurdie, PJ and Holmes, S 2013. Phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS ONE 8, e61217.Google Scholar
Michelland, RJ, Combes, S, Monteils, V, Cauquil, L, Gidenne, T and Fortun-Lamothe, L 2010. Molecular analysis of the bacterial community in digestive tract of rabbit. Anaerobe 16, 61–65.CrossRefGoogle ScholarPubMed
O’Toole, PW and Jeffery, IB 2015. Gut microbiota and aging. Science 350, 1214–1215.Google ScholarPubMed
Odamaki, T, Kato, K, Sugahara, H, Hashikura, N, Takahashi, S, Xiao, J, Abe, F and Osawa, R 2016. Age-related changes in gut microbiota composition from newborn to centenarian: a cross-sectional study. BMC Microbiology 16, 90.CrossRefGoogle ScholarPubMed
Quast, C, Pruesse, E, Yilmaz, P, Gerken, J, Schweer, T, Yarza, P, Peplies, J and Glöckner, FO 2013. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Research 41, D590–D596.CrossRefGoogle ScholarPubMed
Quevedo, F, Pascual, JJ, Blas, E and Cervera, C 2003. Influencia de la madre sobre el crecimiento y la mortalidad de los gazapos en cebo. In XXVIII Symposium de Cunicultura, pp. 115–122. ASESCU, Alcañiz, España.Google Scholar
R Core Team 2019. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Retrieved on 26 April 2019 from http://r-project.orgGoogle Scholar
Rashwan, AA and Marai, IFM 2000. Mortality in young rabbits: a review. World Rabbit Science 8, 111–124.Google Scholar
Read, T, Fortun-Lamothe, L, Pascal, G, Le Boulch, M, Cauquil, L, Gabinaud, B, Bannelier, C, Balmisse, E, Destombes, N, Bouchez, O, Gidenne, T and Combes, S 2019. Diversity and co-occurrence pattern analysis of cecal microbiota establishment at the onset of solid feeding in young rabbits. Frontiers in Microbiology 10, 973.CrossRefGoogle ScholarPubMed
Rodríguez-Romero, N, Abecia, L, Martínez-Vallespín, B and Fondevila, M 2013. Characterisation of caecal microbial diversity of lactating does and their offspring given diets with different neutral detergent soluble to insoluble fibre ratios. Antonie Van Leeuwenhoek 103, 1057–1068.Google ScholarPubMed
Rognes, T, Flouri, T, Nichols, B, Quince, C and Mahé, F 2016. VSEARCH: a versatile open source tool for metagenomics. PeerJ 4, e2584. doi: 10.7717/peerj.2584.CrossRefGoogle ScholarPubMed
Vaiserman, AM, Koliada, AK and Marotta, F 2017. Gut microbiota: a player in aging and a target for anti-aging intervention. Ageing Research Reviews 35, 36–45.Google Scholar
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