Four PQQ-Dependent Alcohol Dehydrogenases Responsible for the Oxidative Detoxification of Deoxynivalenol in a Novel Bacterium Ketogulonicigenium vulgare D3_3 Originated from the Feces of Tenebrio molitor Larvae

Toxins (Basel). 2023 May 30;15(6):367. doi: 10.3390/toxins15060367.

Abstract

Deoxynivalenol (DON) is frequently detected in cereals and cereal-based products and has a negative impact on human and animal health. In this study, an unprecedented DON-degrading bacterial isolate D3_3 was isolated from a sample of Tenebrio molitor larva feces. A 16S rRNA-based phylogenetic analysis and genome-based average nucleotide identity comparison clearly revealed that strain D3_3 belonged to the species Ketogulonicigenium vulgare. This isolate D3_3 could efficiently degrade 50 mg/L of DON under a broad range of conditions, such as pHs of 7.0-9.0 and temperatures of 18-30 °C, as well as during aerobic or anaerobic cultivation. 3-keto-DON was identified as the sole and finished DON metabolite using mass spectrometry. In vitro toxicity tests revealed that 3-keto-DON had lower cytotoxicity to human gastric epithelial cells and higher phytotoxicity to Lemna minor than its parent mycotoxin DON. Additionally, four genes encoding pyrroloquinoline quinone (PQQ)-dependent alcohol dehydrogenases in the genome of isolate D3_3 were identified as being responsible for the DON oxidation reaction. Overall, as a highly potent DON-degrading microbe, a member of the genus Ketogulonicigenium is reported for the first time in this study. The discovery of this DON-degrading isolate D3_3 and its four dehydrogenases will allow microbial strains and enzyme resources to become available for the future development of DON-detoxifying agents for food and animal feed.

Keywords: 3-keto-DON; DON biodegradation; Ketogulonicigenium vulgare; PQQ-dependent alcohol dehydrogenases; toxicity.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Humans
  • Larva
  • Oxidative Stress
  • Oxidoreductases
  • PQQ Cofactor
  • Phylogeny
  • RNA, Ribosomal, 16S / genetics
  • Rhodobacteraceae*
  • Tenebrio*

Substances

  • deoxynivalenol
  • 3-keto-deoxynivalenol
  • PQQ Cofactor
  • RNA, Ribosomal, 16S
  • Oxidoreductases

Supplementary concepts

  • Ketogulonicigenium vulgare

Grants and funding

This research was funded by National Natural Science Foundation of China (Grant No. 31972605) and Key Research and Development Program of Ningxia, China (Grant No. 2022BBF03031).