Associations between the human intestinal microbiota, Lactobacillus rhamnosus GG and serum lipids indicated by integrated analysis of high-throughput profiling data

Leo Lahti; Anne Salonen; Riina A Kekkonen; Jarkko Salojärvi; Jonna Jalanka-Tuovinen; Airi Palva; Matej Orešič; Willem M de Vos

doi:10.7717/peerj.32

Associations between the human intestinal microbiota, Lactobacillus rhamnosus GG and serum lipids indicated by integrated analysis of high-throughput profiling data

PeerJ. 2013 Feb 26:1:e32. doi: 10.7717/peerj.32. Print 2013.

Authors

Leo Lahti^#^{1

2}, Anne Salonen^#^{1

3}, Riina A Kekkonen⁴, Jarkko Salojärvi¹, Jonna Jalanka-Tuovinen¹, Airi Palva¹, Matej Orešič⁵, Willem M de Vos^{1

2

3}

Affiliations

¹ Department of Veterinary Biosciences, University of Helsinki, Finland.
² Laboratory of Microbiology, Wageningen University, Wageningen, Netherlands.
³ Department of Bacteriology and Immunology, Haartman Institute, University of Helsinki, Finland.
⁴ Valio R&D, Helsinki, Finland.
⁵ Quantitative Biology and Bioinformatics, VTT Technical Research Centre of Finland, Espoo, Finland.

^# Contributed equally.

Abstract

Accumulating evidence indicates that the intestinal microbiota regulates our physiology and metabolism. Bacteria marketed as probiotics confer health benefits that may arise from their ability to affect the microbiota. Here high-throughput screening of the intestinal microbiota was carried out and integrated with serum lipidomic profiling data to study the impact of probiotic intervention on the intestinal ecosystem, and to explore the associations between the intestinal bacteria and serum lipids. We performed a comprehensive intestinal microbiota analysis using a phylogenetic microarray before and after Lactobacillus rhamnosus GG intervention. While a specific increase in the L. rhamnosus-related bacteria was observed during the intervention, no other changes in the composition or stability of the microbiota were detected. After the intervention, lactobacilli returned to their initial levels. As previously reported, also the serum lipid profiles remained unaltered during the intervention. Based on a high-resolution microbiota analysis, intake of L. rhamnosus GG did not modify the composition of the intestinal ecosystem in healthy adults, indicating that probiotics confer their health effects by other mechanisms. The most prevailing association between the gut microbiota and lipid profiles was a strong positive correlation between uncultured phylotypes of Ruminococcus gnavus-group and polyunsaturated serum triglycerides of dietary origin. Moreover, a positive correlation was detected between serum cholesterol and Collinsella (Coriobacteriaceae). These associations identified with the spectrometric lipidome profiling were corroborated by enzymatically determined cholesterol and triglyceride levels. Actinomycetaceae correlated negatively with triglycerides of highly unsaturated fatty acids while a set of Proteobacteria showed negative correlation with ether phosphatidylcholines. Our results suggest that several members of the Firmicutes, Actinobacteria and Proteobacteria may be involved in the metabolism of dietary and endogenous lipids, and provide a scientific rationale for further human studies to explore the role of intestinal microbes in host lipid metabolism.

Keywords: Gastrointestinal tract; High-throughput profiling; Lactobacillus rhamnosus GG; Lipidomics; Microbiota; Physiology; Probiotics.

Grants and funding

This work was partly funded by the Finnish Funding Agency for Technology and Innovation (TEKES; grant number 40274/06), the ERC grant Microbes Inside (grant 250172), and the Academy of Finland (grant 137389) to WMdV. We gratefully acknowledge the HITChip team (Wageningen University, NL supported by the Spinoza Award of the Netherlands Foundation for Scientific Research to WMdV) for the HITChip analysis. The work at the University of Helsinki was performed at the Centre of Excellence on Microbial Food Safety Research, Academy of Finland. LL received funding from the Academy of Finland (decision 256950) and Alfred Kordelin Foundation. Support was received from Valio; a manufacturer of probiotics. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.