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

PLoS ONE

Volumn 9, Issue 4, 2014, Pages

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

^a ABERYSTWYTH UNIVERSITY   (United Kingdom)

^b STATE UNIVERSITY OF MARINGÁ   (Brazil)

^c Kyungpook National University   (South Korea)

^d SHERBROOKE RESEARCH AND DEVELOPMENT CENTRE   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL RNA; DNA; ENTEROLACTONE; LIGNAN; RNA 16S; SECOISOLARICIRESINOL; SECOISOLARICIRESINOL DIGLUCOSIDE; UNCLASSIFIED DRUG; ANTIOXIDANT;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BACTERIUM CULTURE; BUTYRIVIBRIO; BUTYRIVIBRIO FIBRISOLVENS; BUTYRIVIBRIO PROTEOCLASTICUS; CONTROLLED STUDY; COW; DNA SEQUENCE; EUBACTERIUM; EUBACTERIUM RUMINANTIUM; FIBROBACTER SUCCINOGENES; FLAX; IN VITRO STUDY; INTESTINE FLORA; NONHUMAN; NUCLEOTIDE SEQUENCE; PEPTOSTREPTOCOCCUS ANAEROBIUS; PHYLOGENETIC TREE; PLANT METABOLISM; PREVOTELLA; PREVOTELLA ALBENSIS; PREVOTELLA BREVIS; PREVOTELLA BRYANTII; PREVOTELLA RUMINICOLA; RUMINANT STOMACH; RUMINOCOCCUS ALBUS; RUMINOCOCCUS FLAVEFACIENS; ANIMAL; BOVINE; FEMALE; GENETICS; HUMAN; ISOLATION AND PURIFICATION; METABOLISM; MICROBIOLOGY; REAL TIME POLYMERASE CHAIN REACTION; RESTRICTION FRAGMENT LENGTH POLYMORPHISM;

ANIMALS; ANTIOXIDANTS; CATTLE; FEMALE; HUMANS; LIGNANS; POLYMORPHISM, RESTRICTION FRAGMENT LENGTH; PREVOTELLA; REAL-TIME POLYMERASE CHAIN REACTION; RNA, RIBOSOMAL, 16S; STOMACH, RUMINANT;

EID: 84899457858     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0087949     Document Type: Article

References (52)

1. Prasad K (1997) Hydroxyl radical-scavenging property of secoisolariciresinol diglucoside (SDG) isolated from flax-seed. Mol Cell Biochem 168: 117-123.
2. Prasad K (2000) Antioxidant activity of secoisolariciresinol diglucoside-derived metabolites, secoisolariciresinol, enterodiol, and enterolactone. Int J Angiol 9: 220-225.
3. Raffaelli B, Hoikkala A, Leppälä E, Wähälä K (2002) Enterolignans. J Chromatogr B 777: 29-43. (Pubitemid 35257860)
4. Hu C, Yuan YV, Kitts DD (2007) Antioxidant activities of the flaxseed lignan secoisolariciresinol diglucoside, its aglycone secoisolariciresinol and the mammalian lignans enterodiol and enterolactone in vitro . Food Chem Toxicol 45: 2219-2227. (Pubitemid 47451575)
5. Jin JS, Hattori M (2011) A new mammalian lignan precursor, asarinin. Food Chem 124: 895-899.
6. Adlercreutz H, Mazur W (1997) Phyto-oestrogens and Western diseases. Ann Med 29: 95-120. (Pubitemid 27226319)
7. Côrtes C, Gagnon N, Benchaar C, Da Silva D, Santos GTD, et al. (2008) In vitro metabolism of flax lignans by ruminal and faecal microbiota of dairy cows. J Appl Microbiol 105: 1585-1594.
8. Clavel T, Borrmann D, Braune A, Doré J, Blaut M (2006) Occurrence and activity of human intestinal bacteria involved in the conversion of dietary lignans. Anaerobe 12: 140-147. (Pubitemid 43831679)
9. Morris DH, Flax Council of Canada (2007) Flax: a health and nutrition primer: Flax Council of Canada.
10. Clavel T, Henderson G, Engst W, Doré J, Blaut M (2006) Phylogeny of human intestinal bacteria that activate the dietary lignan secoisolariciresinol diglucoside. FEMS Microbiol Ecol 55: 471-478.
11. Wang LQ, Meselhy MR, Li Y, Qin GW, Hattori M (2000) Human intestinal bacteria capable of transforming secoisolariciresinol diglucoside to mammalian lignans, enterodiol and enterolactone. Chem Pharm Bull 48: 1606-1610.
12. Wang CZ, Ma XQ, Yang DH, Guo ZR, Liu GR, et al. (2010) Production of enterodiol from defatted flaxseeds through biotransformation by human intestinal bacteria. BMC Microbiol 10: 115.
13. Clavel T, Henderson G, Alpert CA, Philippe C, Rigottier-Gois L, et al. (2005) Intestinal bacterial communities that produce active estrogen-like compounds enterodiol and enterolactone in humans. Appl Environ Microbiol 71: 6077-6085. (Pubitemid 41456904)
14. Wang LQ (2002) Mammalian phytoestrogens: enterodiol and enterolactone. J Chromatogr B 777: 289-309.
15. Petit HV, Gagnon N (2009) Milk concentrations of the mammalian lignans enterolactone and enterodiol, milk production, and whole tract digestibility of dairy cows fed diets containing different concentrations of flaxseed meal. Anim Feed Sci Tech 152: 103-111.
16. Petit HV, Gagnon N (2009) Concentration of the mammalian lignans enterolactone and enterodiol in milk of cows fed diets containing different concentrations of whole flaxseed. Animal 3: 1428-1435.
17. Zhou W, Wang G, Han Z, Yao W, Zhu W (2009) Metabolism of flaxseed lignans in the rumen and its impact on ruminal metabolism and flora. Anim Feed Sci Tech 150: 18-26.
18. Gagnon N, Côrtes C, da Silva D, Kazama R, Benchaar C, et al. (2009) Ruminal metabolism of flaxseed (Linum usitatissimum) lignans to the mammalian lignan enterolactone and its concentration in ruminal fluid, plasma, urine and milk of dairy cows. Brit J Nutr 102: 1015-1023.
19. Gagnon N, Côrtes C, Petit HV (2009) Weekly excretion of the mammalian lignan enterolactone in milk of dairy cows fed flaxseed meal. J Dairy Res 76: 455-458.
20. Petit HV, Gagnon N, Mir PS, Cao R, Cui S (2009) Milk concentration of the mammalian lignan enterolactone, milk production, milk fatty acid profile, and digestibility in dairy cows fed diets containing whole flaxseed or flaxseed meal. J Dairy Res 76: 257-264.
21. Petit HV, Gagnon N (2011) Production performance and milk composition of dairy cows fed different concentrations of flax hulls. Anim Feed Sci Tech 169: 46-52.
22. Matumoto-Pintro PT, Petit HV, Giroux HJ, Côrtes C, Gagnon N, et al. (2011) Effect of flaxseed lignans added to milk or fed to cows on oxidative degradation of dairy beverages enriched with polyunsaturated fatty acids. J Dairy Res 78: 111-117.
23. Canadian Council on Animal Care (1993) Guide to the Care and Use of Experimental Animals; Offert ED, Cross BM, McWilliam AA, editors. Ottawa: Canada: CCAC.
24. National Research Council (2001) Nutrient Requirements of Dairy Cattle: Seventh Revised Edition, 2001: The National Academies Press.
25. Lee M, Harris L, Moorby J, Humphreys M, Theodorou M, et al. (2002) Rumen metabolism and nitrogen flow to the small intestine in steers offered Lolium perenne containing different levels of water-soluble carbohydrate. J Anim Sci 74: 587-596. (Pubitemid 34853682)
26. Huws SA, Kim EJ, Lee MRF, Scott MB, Tweed JKS, et al. (2011) As yet uncultured bacteria phylogenetically classified as Prevotella, Lachnospiraceae incertae sedis and unclassified Bacteroidales, Clostridiales and Ruminococcaceae may play a predominant role in ruminal biohydrogenation. Environ Microbiol 13: 1500-1512.
27. Huws SA, Scott MB, Tweed JKS, Lee MRF (2013) Fatty acid oxidation products ('green odour') released from perennial ryegrass following biotic and abiotic stress, potentially have antimicrobial properties against the rumen microbiota resulting in decreased biohydrogenation. J Appl Microbiol 115: 1081-1090.
28. Blackwood CB, Marsh T, Kim SH, Paul EA (2003) Terminal restriction fragment length polymorphism data analysis for quantitative comparison of microbial communities. Appl Environ Microbiol 69: 926-932. (Pubitemid 36204820)
29. Huws SA, Edwards JE, Kim EJ, Scollan ND (2007) Specificity and sensitivity of eubacterial primers utilized for molecular profiling of bacteria within complex microbial ecosystems. J Microbiol Meth 70: 565-569. (Pubitemid 47307374)
30. Huws SA, Mayorga OL, Theodorou MK, Onime LA, Kim EJ, et al. (2013) Successional colonization of perennial ryegrass by rumen bacteria. Lett Appl Microbiol 56: 186-196.
31. Kim EJ, Huws SA, Lee MRF, Wood JD, Muetzel SM, et al. (2008) Fish oil increases the duodenal flow of long chain polyunsaturated fatty acids and trans-11 18:1 and decreases 18:0 in steers via changes in the rumen bacterial community. J Nutr 138: 889-896. (Pubitemid 351571588)
32. Sanguinetti CJ, Dias Neto E, Simpson AJ (1994) Rapid silver staining and recovery of PCR products separated on polyacrylamide gels. Biotechniques 17: 914-921.
33. Cole JR, Chai B, Farris RJ, Wang Q, Kulam SA, et al. (2005) The Ribosomal Database Project (RDP-II): sequences and tools for high-throughput rRNA analysis. Nucleic Acids Res 33: D294-D296. (Pubitemid 40207881)
34. Hobson PN (1969) Rumen bacteria. Methods Microbiology 3B: 133-149.
35. Nesbitt PD, Lam Y, Thompson LU (1999) Human metabolism of mammalian lignan precursors in raw and processed flaxseed. Am J Clin Nutr 69: 549-555. (Pubitemid 29104580)
36. Côrtes C, da Silva-Kazama D, Kazama R, Benchaar C, dos Santos G, et al. (2013) Effects of abomasal infusion of flaxseed (Linum usitatissimum) oil on microbial b-glucuronidase activity and concentration of the mammalian lignan enterolactone in ruminal fluid, plasma, urine and milk of dairy cows. Brit J Nutr 109: 433-440.
37. Penalvo JL, Haajanen KM, Botting N, Adlercreutz H (2005) Quantification of lignans in food using isotope dilution gas chromatography/mass spectrometry. J Agr Food Chem 53: 9342-9347. (Pubitemid 41784134)
38. Steinshamn H, Purup S, Thuen E, Hansen-Müller J (2008) Effects of clover-grass silages and concentrate supplementation on the content of phytoestrogens in dairy cow milk. J Dairy Sci 91: 2715-2725. (Pubitemid 351976594)
39. Thompson LU, Robb P, Serraino M, Cheung F (1991) Mammalian lignan production from various foods. Nutr Cancer 16: 43-52.
40. Smalla K, Oros-Sichler M, Milling A, Heuer H, Baumgarte S, et al. (2007) Bacterial diversity of soils assessed by DGGE, T-RFLP and SSCP fingerprints of PCR-amplified 16S rRNA gene fragments: Do the different methods provide similar results? J Microbiol Meth 69: 470-479. (Pubitemid 46691255)
41. Casamayor EO, Massana R, Benlloch S, Øvreås L, Díez B, et al. (2002) Changes in archaeal, bacterial and eukaryal assemblages along a salinity gradient by comparison of genetic fingerprinting methods in a multipond solar saltern. Environ Microbiol 4: 338-348. (Pubitemid 34788806)
42. Enwall K, Hallin S (2009) Comparison of T-RFLP and DGGE techniques to assess denitrifier community composition in soil. Lett Appl Microbiol 48: 145-148.
43. 2-glucuronidase enzyme from a human intestinal bacterium, Ruminococcus gnavus. Microbiology 151: 2323-2330.
44. Heinonen S, Nurmi T, Liukkonen K, Poutanen K, Wähälä K, et al. (2001) In vitro metabolism of plant lignans: new precursors of mammalian lignans enterolactone and enterodiol. J Agr Food Chem 49: 3178-3186. (Pubitemid 32845044)
45. Landete JM (2012) Plant and mammalian lignans: A review of source, intake, metabolism, intestinal bacteria and health. Food Res Int 46: 410-424.
46. Krause DO, Denman SE, Mackie RI, Morrison M, Rae AL, et al. (2003) Opportunities to improve fiber degradation in the rumen: microbiology, ecology, and genomics. FEMS Microbiol Rev 27: 663-693. (Pubitemid 37456863)
47. Antignac JP, Cariou R, Bizec BL, André F (2004) New data regarding phytoestrogens content in bovine milk. Food Chem 87: 275-281. (Pubitemid 38581905)
48. Höjer A, Adler S, Purup S, Hansen-Müller J, Martinsson K, et al. (2012) Effects of feeding dairy cows different legume-grass silages on milk phytoestrogen concentration. J Dairy Sci 95: 4526-4540.
49. Aura AM, Oikarinen S, Mutanen M, Heinonen SM, Adlercreutz HCT, et al. (2006) Suitability of a batch in vitro fermentation model using human faecal microbiota for prediction of conversion of flaxseed lignans to enterolactone with reference to an in vivo rat model. Eur J Nutr 45: 45-51. (Pubitemid 43221283)
50. Liu Z, Saarinen NM, Thompson LU (2006) Sesamin is one of the major precursors of mammalian lignans in sesame seed (Sesamum indicum) as observed in vitro and in rats. JNutr 136: 906-912.
51. Borriello SP, Setchell KDR, Axelson M, Lawson AM (1985) Production and metabolism of lignans by the human faecal flora. J Appl Bacteriol 58: 37-43. (Pubitemid 15136128)
52. Holma R, Kekkonen RA, Hatakka K, Poussa T, Vapaatalo H, et al. (2013) Low serum enterolactone concentration is associated with low colonic Lactobacillus-Enterococcus counts in men but is not affected by a synbiotic mixture in a randomised, placebo-controlled, double-blind, cross-over intervention study. Brit J Nutr 7: 1-9.