Colonic Bacteroides are positively associated with trabecular bone structure and programmed by maternal vitamin D in male but not female offspring in an obesogenic environment

Abstract

Background/Objectives:

The gut microbiota is determined early in life, possibly including pregnancy. Pioneering data suggest vitamin D, a nutrient important for bone health, affects this microbiota. We found that high maternal vitamin D lowered circulating lipopolysaccharide (LPS), improved intestinal barrier and bone health in male but not female offspring in an obesogenic environment. This study determined if high maternal dietary vitamin D programs Bacteroides and Prevotella and whether this associates with bone mineral content, density and structure of male and female adult offspring fed an obesogenic diet.

Methods:

C57BL/6J females received an AIN93G diet with high or low vitamin D from before mating until weaning. Post-weaning, male and female offspring remained on their respective vitamin D level or were switched and fed a high fat and sucrose diet until killing (age 7 months). Bacteroides and Prevotella were quantified in dams’ feces and offspring colonic contents. LPS concentrations, bone mineral density and content, strength and structure data were integrated from our previous studies in the same mice. Spearman correlations were completed between Bacteroides and LPS, and bone outcomes.

Results:

There was a maternal vitamin D effect on colonic Bacteroides but not Prevotella (dam diet: <0.001 and 0.735) in adult male offspring, independent of dams fecal Bacteroides before birth (P=0.998). In males, but not females, Bacteroides correlated with LPS (r=−0.488, P=0.018), trabecular femur peak load (r=0.362, P=0.033), vertebral trabecular separation (r=−0.605, P=0.006), trabecular number (r=0.614, P=0.005) and bone volume fraction (r=0.549, P=0.015).

Conclusions:

Dietary vitamin D programs Bacteroides in male adult offspring only, which correlated negatively with systemic inflammation and positively with bone strength and structure. This may have implications on maternal diet and nutritional guidelines targeting sexes in a different manner.

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Acknowledgements

We thank Shivani Kasee for technical help. This project was funded by a matching grant from the Centrum Foundation of Pfizer Consumer Healthcare Research Innovation Fund and the Department of Nutritional Sciences at the University of Toronto to EMC and WEW and from a Natural Sciences and Engineering Research Council of Canada (NSERC) Discovery grant to EMC (grant # RGPIN 356124-2013). The μCT system was purchased with funding from the Canada Foundation for Innovation to WEW (grant #222084). CRV was partially funded by the Banting and Best Diabetes Centre–Novo Nordisk Studentship and –Tamarack Graduate Award in Diabetes Research and by an Ontario Graduate Scholarship. WEW holds a Canada Research Chair in Bone and Muscle Development at Brock University. EMC holds the Lawson Family Chair in Microbiome Nutrition Research at the University of Toronto.

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Correspondence to E M Comelli.

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Villa, C., Taibi, A., Chen, J. et al. Colonic Bacteroides are positively associated with trabecular bone structure and programmed by maternal vitamin D in male but not female offspring in an obesogenic environment. Int J Obes 42, 696–703 (2018). https://doi.org/10.1038/ijo.2017.294

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