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Open Access Highly Accessed Research article

Toxicity of unsaturated fatty acids to the biohydrogenating ruminal bacterium, Butyrivibrio fibrisolvens

Margarida RG Maia124, Lal C Chaudhary15, Charles S Bestwick1, Anthony J Richardson1, Nest McKain1, Tony R Larson3, Ian A Graham3 and Robert J Wallace1*

Author affiliations

1 Rowett Institute of Nutrition and Health, University of Aberdeen, Bucksburn, Aberdeen AB21 9SB, UK

2 Unidade de Produção Animal, Instituto Nacional de Recursos Biológicos, Fonte Boa, 2005-048 Vale de Santarém, Portugal

3 Department of Biology, University of York, PO Box 373, York YO10 5YW, UK

4 Current address: Requimte, ICBAS, Instituto de Ciências Biomédicas Abel Salazar, Universidade do Porto, Campus Agrário de Vairão, Rua Padre Armando Quintas, 4485-661 Vairão VC, Portugal

5 Current address: Centre of Advanced Studies in Animal Nutrition, Indian Veterinary Research Institute, Izatnagar - 243 122, India

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Citation and License

BMC Microbiology 2010, 10:52  doi:10.1186/1471-2180-10-52

Published: 18 February 2010

Abstract

Background

Health-promoting polyunsaturated fatty acids (PUFA) are abundant in forages grazed by ruminants and in vegetable and fish oils used as dietary supplements, but only a small proportion of PUFA finds its way into meat and milk, because of biohydrogenation in the rumen. Butyrivibrio fibrisolvens plays a major role in this activity. The aim of this study was to investigate the mechanisms by which PUFA affect the growth of B. fibrisolvens, how PUFA are metabolized and the metabolic response to growth in the presence of PUFA.

Results

Linoleic acid (LA; cis-9, cis-12-18:2) and α-linolenic acid (LNA; cis-9, cis-12, cis-15-18:3) increased the lag phase of B. fibrisolvens JW11, LNA having the greater effect. Growth was initiated only when the PUFA had been converted to vaccenic acid (VA; trans-11-18:1). The major fish oil fatty acids, eicosapentaenoic acid (EPA; 20:5(n-3)) and docosahexaenoic acid (DHA; 22:6(n-3)), were not metabolized and prevented growth. Cellular integrity, as determined fluorimetrically by propidium iodide (PI) ingression, was affected as much by 18:1 fatty acids, including VA, as 18:2 fatty acids. The methyl esters of LNA, LA, EPA and DHA had no effect on growth or other measurements. The ATP pool decreased by 2/3 when LA was added to growing bacteria, whereas most acyl CoA pools decreased by >96%.

Conclusions

It was concluded that biohydrogenation occurs to enable B. fibrisolvens to survive the bacteriostatic effects of PUFA, and that the toxicity of PUFA is probably mediated via a metabolic effect rather than disruption of membrane integrity.