Ruminal Prevotella spp. may play an important role in the conversion of plant lignans into human health beneficial antioxidants

Ana L B Schogor, Sharon A Huws, Geraldo T D Santos, Nigel D Scollan, Barbara D Hauck, Ana L Winters, Eun J Kim, Hélène V Petit

Research output: Contribution to journalArticle

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Abstract

Secoisolariciresinol diglucoside (SDG), the most abundant lignan in flaxseed, is metabolized by the ruminal microbiota into enterolignans, which are strong antioxidants. Enterolactone (EL), the main mammalian enterolignan produced in the rumen, is transferred into physiological fluids, with potentially human health benefits with respect to menopausal symptoms, hormone-dependent cancers, cardiovascular diseases, osteoporosis and diabetes. However, no information exists to our knowledge on bacterial taxa that play a role in converting plant lignans into EL in ruminants. In order to investigate this, eight rumen cannulated cows were used in a double 4 × 4 Latin square design and fed with four treatments: control with no flax meal (FM), or 5%, 10% and 15% FM (on a dry matter basis). Concentration of EL in the rumen increased linearly with increasing FM inclusion. Total rumen bacterial 16S rRNA concentration obtained using Q-PCR did not differ among treatments. PCR-T-RFLP based dendrograms revealed no global clustering based on diet indicating between animal variation. PCR-DGGE showed a clustering by diet effect within four cows that had similar basal ruminal microbiota. DNA extracted from bands present following feeding 15% FM and absent with no FM supplementation were sequenced and it showed that many genera, in particular Prevotella spp., contributed to the metabolism of lignans. A subsequent in vitro study using selected pure cultures of ruminal bacteria incubated with SDG indicated that 11 ruminal bacteria were able to convert SDG into secoisolariciresinol (SECO), with Prevotella spp. being the main converters. These data suggest that Prevotella spp. is one genus playing an important role in the conversion of plant lignans to human health beneficial antioxidants in the rumen.

Original languageEnglish
Article numbere87949
JournalPloS one
Volume9
Issue number4
DOIs
Publication statusPublished - 07 Apr 2014

Fingerprint

Prevotella
Flax
Lignans
flax
lignans
Rumen
human health
rumen
Antioxidants
Meals
Health
antioxidants
rumen bacteria
Nutrition
Microbiota
Bacteria
Polymerase Chain Reaction
Cluster Analysis
cows
menopause

Keywords

  • Animals
  • Antioxidants
  • Cattle
  • Female
  • Humans
  • Lignans
  • Polymorphism, Restriction Fragment Length
  • Prevotella
  • RNA, Ribosomal, 16S
  • Real-Time Polymerase Chain Reaction
  • Stomach, Ruminant
  • Journal Article
  • Research Support, Non-U.S. Gov't

Cite this

Schogor, Ana L B ; Huws, Sharon A ; Santos, Geraldo T D ; Scollan, Nigel D ; Hauck, Barbara D ; Winters, Ana L ; Kim, Eun J ; Petit, Hélène V. / Ruminal Prevotella spp. may play an important role in the conversion of plant lignans into human health beneficial antioxidants. In: PloS one. 2014 ; Vol. 9, No. 4.
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abstract = "Secoisolariciresinol diglucoside (SDG), the most abundant lignan in flaxseed, is metabolized by the ruminal microbiota into enterolignans, which are strong antioxidants. Enterolactone (EL), the main mammalian enterolignan produced in the rumen, is transferred into physiological fluids, with potentially human health benefits with respect to menopausal symptoms, hormone-dependent cancers, cardiovascular diseases, osteoporosis and diabetes. However, no information exists to our knowledge on bacterial taxa that play a role in converting plant lignans into EL in ruminants. In order to investigate this, eight rumen cannulated cows were used in a double 4 × 4 Latin square design and fed with four treatments: control with no flax meal (FM), or 5{\%}, 10{\%} and 15{\%} FM (on a dry matter basis). Concentration of EL in the rumen increased linearly with increasing FM inclusion. Total rumen bacterial 16S rRNA concentration obtained using Q-PCR did not differ among treatments. PCR-T-RFLP based dendrograms revealed no global clustering based on diet indicating between animal variation. PCR-DGGE showed a clustering by diet effect within four cows that had similar basal ruminal microbiota. DNA extracted from bands present following feeding 15{\%} FM and absent with no FM supplementation were sequenced and it showed that many genera, in particular Prevotella spp., contributed to the metabolism of lignans. A subsequent in vitro study using selected pure cultures of ruminal bacteria incubated with SDG indicated that 11 ruminal bacteria were able to convert SDG into secoisolariciresinol (SECO), with Prevotella spp. being the main converters. These data suggest that Prevotella spp. is one genus playing an important role in the conversion of plant lignans to human health beneficial antioxidants in the rumen.",
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Ruminal Prevotella spp. may play an important role in the conversion of plant lignans into human health beneficial antioxidants. / Schogor, Ana L B; Huws, Sharon A; Santos, Geraldo T D; Scollan, Nigel D; Hauck, Barbara D; Winters, Ana L; Kim, Eun J; Petit, Hélène V.

In: PloS one, Vol. 9, No. 4, e87949, 07.04.2014.

Research output: Contribution to journalArticle

TY - JOUR

T1 - Ruminal Prevotella spp. may play an important role in the conversion of plant lignans into human health beneficial antioxidants

AU - Schogor, Ana L B

AU - Huws, Sharon A

AU - Santos, Geraldo T D

AU - Scollan, Nigel D

AU - Hauck, Barbara D

AU - Winters, Ana L

AU - Kim, Eun J

AU - Petit, Hélène V

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N2 - Secoisolariciresinol diglucoside (SDG), the most abundant lignan in flaxseed, is metabolized by the ruminal microbiota into enterolignans, which are strong antioxidants. Enterolactone (EL), the main mammalian enterolignan produced in the rumen, is transferred into physiological fluids, with potentially human health benefits with respect to menopausal symptoms, hormone-dependent cancers, cardiovascular diseases, osteoporosis and diabetes. However, no information exists to our knowledge on bacterial taxa that play a role in converting plant lignans into EL in ruminants. In order to investigate this, eight rumen cannulated cows were used in a double 4 × 4 Latin square design and fed with four treatments: control with no flax meal (FM), or 5%, 10% and 15% FM (on a dry matter basis). Concentration of EL in the rumen increased linearly with increasing FM inclusion. Total rumen bacterial 16S rRNA concentration obtained using Q-PCR did not differ among treatments. PCR-T-RFLP based dendrograms revealed no global clustering based on diet indicating between animal variation. PCR-DGGE showed a clustering by diet effect within four cows that had similar basal ruminal microbiota. DNA extracted from bands present following feeding 15% FM and absent with no FM supplementation were sequenced and it showed that many genera, in particular Prevotella spp., contributed to the metabolism of lignans. A subsequent in vitro study using selected pure cultures of ruminal bacteria incubated with SDG indicated that 11 ruminal bacteria were able to convert SDG into secoisolariciresinol (SECO), with Prevotella spp. being the main converters. These data suggest that Prevotella spp. is one genus playing an important role in the conversion of plant lignans to human health beneficial antioxidants in the rumen.

AB - Secoisolariciresinol diglucoside (SDG), the most abundant lignan in flaxseed, is metabolized by the ruminal microbiota into enterolignans, which are strong antioxidants. Enterolactone (EL), the main mammalian enterolignan produced in the rumen, is transferred into physiological fluids, with potentially human health benefits with respect to menopausal symptoms, hormone-dependent cancers, cardiovascular diseases, osteoporosis and diabetes. However, no information exists to our knowledge on bacterial taxa that play a role in converting plant lignans into EL in ruminants. In order to investigate this, eight rumen cannulated cows were used in a double 4 × 4 Latin square design and fed with four treatments: control with no flax meal (FM), or 5%, 10% and 15% FM (on a dry matter basis). Concentration of EL in the rumen increased linearly with increasing FM inclusion. Total rumen bacterial 16S rRNA concentration obtained using Q-PCR did not differ among treatments. PCR-T-RFLP based dendrograms revealed no global clustering based on diet indicating between animal variation. PCR-DGGE showed a clustering by diet effect within four cows that had similar basal ruminal microbiota. DNA extracted from bands present following feeding 15% FM and absent with no FM supplementation were sequenced and it showed that many genera, in particular Prevotella spp., contributed to the metabolism of lignans. A subsequent in vitro study using selected pure cultures of ruminal bacteria incubated with SDG indicated that 11 ruminal bacteria were able to convert SDG into secoisolariciresinol (SECO), with Prevotella spp. being the main converters. These data suggest that Prevotella spp. is one genus playing an important role in the conversion of plant lignans to human health beneficial antioxidants in the rumen.

KW - Animals

KW - Antioxidants

KW - Cattle

KW - Female

KW - Humans

KW - Lignans

KW - Polymorphism, Restriction Fragment Length

KW - Prevotella

KW - RNA, Ribosomal, 16S

KW - Real-Time Polymerase Chain Reaction

KW - Stomach, Ruminant

KW - Journal Article

KW - Research Support, Non-U.S. Gov't

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DO - 10.1371/journal.pone.0087949

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JF - PLoS One

SN - 1932-6203

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