Porcine small and large intestinal microbiota rapidly hydrolyze the masked mycotoxin deoxynivalenol-3-glucoside and release deoxynivalenol in spiked batch cultures in vitro

Silvia Gratz, Valerie Currie, Anthony Richardson, Gary Duncan, Grietje Holtrop, Freda Farquharson, Petra Louis, Philippe Pinton, Isabelle P. Oswald

Research output: Contribution to journalArticle

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Abstract

Mycotoxin contamination of cereal grains causes well-recognized toxicities in animals and humans, but the fate of plant-bound masked mycotoxins in the gut is less well understood. Masked mycotoxins have been found to be stable under conditions prevailing in the small intestine, but are rapidly hydrolyzed by fecal microbiota. This study aims to assess the hydrolysis of the masked mycotoxin deoxynivalenol-3-glucoside (DON3Glc) by microbiota of different regions of the porcine intestinal tract.

Intestinal digesta samples were collected from the jejunum, ileum, caecum, colon and feces of 5 pigs and immediately frozen under anaerobic conditions. Sample slurries were prepared in M2 culture medium, spiked with DON3Glc or free DON (2 nmoles/mL) and incubated anaerobically for up to 72 hours. Mycotoxin concentrations were determined using LC-MS/MS and microbiota composition was determined using qPCR methodology.

Jejunal microbiota hydrolyzed DON3Glc very slowly, while samples from the ileum, caecum, colon and feces rapidly and efficiently hydrolyzed DON3Glc. No further metabolism of DON was observed in any sample. Microbial load and microbiota composition was significantly different in the ileum, but similar in caecum, colon and feces.

Importance

Results from this study clearly demonstrate that the masked mycotoxin DON3Glc is hydrolyzed efficiently in the distal small intestine and large intestine of pigs. Once DON is released, toxicity and absorption in the distal intestinal tract are likely to occur in vivo. This study further supports the need to include masked metabolites into mycotoxin risk assessments and regulatory actions for feed and food.
Original languageEnglish
Article number02106-17
Pages (from-to)1-9
Number of pages9
JournalApplied and Environmental Microbiology
Volume84
Issue number2
Early online date3 Nov 2017
DOIs
Publication statusPublished - Jan 2018

Fingerprint

deoxynivalenol-3-glucoside
Batch Cell Culture Techniques
Mycotoxins
deoxynivalenol
intestinal microorganisms
in vitro culture
feces
mycotoxins
Microbiota
Swine
pig
swine
toxicity
Ileum
ileum
Feces
cecum
colon
Colon
anoxic conditions

Keywords

  • deoxynivalenol - 3 -glucoside
  • pig
  • microbiota
  • masked mycotoxin
  • release
  • toxicity
  • trichothecene

Cite this

Porcine small and large intestinal microbiota rapidly hydrolyze the masked mycotoxin deoxynivalenol-3-glucoside and release deoxynivalenol in spiked batch cultures in vitro. / Gratz, Silvia; Currie, Valerie; Richardson, Anthony; Duncan, Gary; Holtrop, Grietje; Farquharson, Freda; Louis, Petra; Pinton, Philippe; Oswald, Isabelle P.

In: Applied and Environmental Microbiology, Vol. 84, No. 2, 02106-17, 01.2018, p. 1-9.

Research output: Contribution to journalArticle

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abstract = "Mycotoxin contamination of cereal grains causes well-recognized toxicities in animals and humans, but the fate of plant-bound masked mycotoxins in the gut is less well understood. Masked mycotoxins have been found to be stable under conditions prevailing in the small intestine, but are rapidly hydrolyzed by fecal microbiota. This study aims to assess the hydrolysis of the masked mycotoxin deoxynivalenol-3-glucoside (DON3Glc) by microbiota of different regions of the porcine intestinal tract.Intestinal digesta samples were collected from the jejunum, ileum, caecum, colon and feces of 5 pigs and immediately frozen under anaerobic conditions. Sample slurries were prepared in M2 culture medium, spiked with DON3Glc or free DON (2 nmoles/mL) and incubated anaerobically for up to 72 hours. Mycotoxin concentrations were determined using LC-MS/MS and microbiota composition was determined using qPCR methodology.Jejunal microbiota hydrolyzed DON3Glc very slowly, while samples from the ileum, caecum, colon and feces rapidly and efficiently hydrolyzed DON3Glc. No further metabolism of DON was observed in any sample. Microbial load and microbiota composition was significantly different in the ileum, but similar in caecum, colon and feces.ImportanceResults from this study clearly demonstrate that the masked mycotoxin DON3Glc is hydrolyzed efficiently in the distal small intestine and large intestine of pigs. Once DON is released, toxicity and absorption in the distal intestinal tract are likely to occur in vivo. This study further supports the need to include masked metabolites into mycotoxin risk assessments and regulatory actions for feed and food.",
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author = "Silvia Gratz and Valerie Currie and Anthony Richardson and Gary Duncan and Grietje Holtrop and Freda Farquharson and Petra Louis and Philippe Pinton and Oswald, {Isabelle P.}",
note = "This study was supported by the Scottish Government Rural and Environment Science and Analytical Services division (RESAS) and by the French Agence Nationale de la Recherche (project ANR-13-CESA-0003-03). We thank Anne-Marie Cossalter for her excellent technical assistance with pigs.",
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AU - Currie, Valerie

AU - Richardson, Anthony

AU - Duncan, Gary

AU - Holtrop, Grietje

AU - Farquharson, Freda

AU - Louis, Petra

AU - Pinton, Philippe

AU - Oswald, Isabelle P.

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N2 - Mycotoxin contamination of cereal grains causes well-recognized toxicities in animals and humans, but the fate of plant-bound masked mycotoxins in the gut is less well understood. Masked mycotoxins have been found to be stable under conditions prevailing in the small intestine, but are rapidly hydrolyzed by fecal microbiota. This study aims to assess the hydrolysis of the masked mycotoxin deoxynivalenol-3-glucoside (DON3Glc) by microbiota of different regions of the porcine intestinal tract.Intestinal digesta samples were collected from the jejunum, ileum, caecum, colon and feces of 5 pigs and immediately frozen under anaerobic conditions. Sample slurries were prepared in M2 culture medium, spiked with DON3Glc or free DON (2 nmoles/mL) and incubated anaerobically for up to 72 hours. Mycotoxin concentrations were determined using LC-MS/MS and microbiota composition was determined using qPCR methodology.Jejunal microbiota hydrolyzed DON3Glc very slowly, while samples from the ileum, caecum, colon and feces rapidly and efficiently hydrolyzed DON3Glc. No further metabolism of DON was observed in any sample. Microbial load and microbiota composition was significantly different in the ileum, but similar in caecum, colon and feces.ImportanceResults from this study clearly demonstrate that the masked mycotoxin DON3Glc is hydrolyzed efficiently in the distal small intestine and large intestine of pigs. Once DON is released, toxicity and absorption in the distal intestinal tract are likely to occur in vivo. This study further supports the need to include masked metabolites into mycotoxin risk assessments and regulatory actions for feed and food.

AB - Mycotoxin contamination of cereal grains causes well-recognized toxicities in animals and humans, but the fate of plant-bound masked mycotoxins in the gut is less well understood. Masked mycotoxins have been found to be stable under conditions prevailing in the small intestine, but are rapidly hydrolyzed by fecal microbiota. This study aims to assess the hydrolysis of the masked mycotoxin deoxynivalenol-3-glucoside (DON3Glc) by microbiota of different regions of the porcine intestinal tract.Intestinal digesta samples were collected from the jejunum, ileum, caecum, colon and feces of 5 pigs and immediately frozen under anaerobic conditions. Sample slurries were prepared in M2 culture medium, spiked with DON3Glc or free DON (2 nmoles/mL) and incubated anaerobically for up to 72 hours. Mycotoxin concentrations were determined using LC-MS/MS and microbiota composition was determined using qPCR methodology.Jejunal microbiota hydrolyzed DON3Glc very slowly, while samples from the ileum, caecum, colon and feces rapidly and efficiently hydrolyzed DON3Glc. No further metabolism of DON was observed in any sample. Microbial load and microbiota composition was significantly different in the ileum, but similar in caecum, colon and feces.ImportanceResults from this study clearly demonstrate that the masked mycotoxin DON3Glc is hydrolyzed efficiently in the distal small intestine and large intestine of pigs. Once DON is released, toxicity and absorption in the distal intestinal tract are likely to occur in vivo. This study further supports the need to include masked metabolites into mycotoxin risk assessments and regulatory actions for feed and food.

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KW - release

KW - toxicity

KW - trichothecene

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SN - 0099-2240

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