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Applied and Environmental Microbiology, June 2009, p. 4175-4184, Vol. 75, No. 12
0099-2240/09/$08.00+0     doi:10.1128/AEM.00380-09
Copyright © 2009, American Society for Microbiology. All Rights Reserved.

Diet-Induced Metabolic Improvements in a Hamster Model of Hypercholesterolemia Are Strongly Linked to Alterations of the Gut Microbiota ^,

Inés Martínez,^1, Grant Wallace,^1, Chaomei Zhang,¹ Ryan Legge,¹ Andrew K. Benson,¹ Timothy P. Carr,² Etsuko N. Moriyama,³ and Jens Walter^1*

Department of Food Science and Technology,¹ Department of Nutrition and Health Sciences, University of Nebraska, Lincoln, Nebraska 68583-0919,² School of Biological Sciences and Center for Plant Science Innovation, University of Nebraska, Lincoln, Nebraska 68588-0118³

Received 16 February 2009/ Accepted 21 April 2009

The mammalian gastrointestinal microbiota exerts a strong influence on host lipid and cholesterol metabolism. In this study, we have characterized the interplay among diet, gut microbial ecology, and cholesterol metabolism in a hamster model of hypercholesterolemia. Previous work in this model had shown that grain sorghum lipid extract (GSL) included in the diet significantly improved the high-density lipoprotein (HDL)/non-HDL cholesterol equilibrium (T. P. Carr, C. L. Weller, V. L. Schlegel, S. L. Cuppett, D. M. Guderian, Jr., and K. R. Johnson, J. Nutr. 135:2236-2240, 2005). Molecular analysis of the hamsters' fecal bacterial populations by pyrosequencing of 16S rRNA tags, PCR-denaturing gradient gel electrophoresis, and Bifidobacterium-specific quantitative real-time PCR revealed that the improvements in cholesterol homeostasis induced through feeding the hamsters GSL were strongly associated with alterations of the gut microbiota. Bifidobacteria, which significantly increased in abundance in hamsters fed GSL, showed a strong positive association with HDL plasma cholesterol levels (r = 0.75; P = 0.001). The proportion of members of the family Coriobacteriaceae decreased when the hamsters were fed GSL and showed a high positive association with non-HDL plasma cholesterol levels (r = 0.84; P = 0.0002). These correlations were more significant than those between daily GSL intake and animal metabolic markers, implying that the dietary effects on host cholesterol metabolism are conferred, at least in part, through an effect on the gut microbiota. This study provides evidence that modulation of the gut microbiota-host metabolic interrelationship by dietary intervention has the potential to improve mammalian cholesterol homeostasis, which has relevance for cardiovascular health.

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* Corresponding author. Mailing address: Department of Food Science and Technology, University of Nebraska, 333 Food Industry Complex, Lincoln, NE 68583-0919. Phone: (402) 472-2615. Fax: (402) 472-1693. E-mail: jwalter2{at}unl.edu

Published ahead of print on 1 May 2009.

Supplemental material for this article may be found at http://aem.asm.org/.

These authors contributed equally to this work.

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Applied and Environmental Microbiology, June 2009, p. 4175-4184, Vol. 75, No. 12
0099-2240/09/$08.00+0     doi:10.1128/AEM.00380-09
Copyright © 2009, American Society for Microbiology. All Rights Reserved.