Cited by 55Redox biology and oxidative stressProbiotics and Fermented FoodsBacterial Genetics and Biotechnology

Influence of Oxygen on NADH Recycling and Oxidative Stress Resistance Systems in Lactobacillus panis PM1

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Kang, Tae Sun, Korber, Darren R, Tanaka, Takuji·2013·AMB Express

Abstract

Lactobacillus panis strain PM1 is an obligatory heterofermentative and aerotolerant microorganism that also produces 1,3-propanediol from glycerol. This study investigated the metabolic responses of L. panis PM1 to oxidative stress under aerobic conditions. Growth under aerobic culture triggered an early entrance of L. panis PM1 into the stationary phase along with marked changes in end-product profiles. A ten-fold higher concentration of hydrogen peroxide was accumulated during aerobic culture compared to microaerobic culture. This H2O2 level was sufficient for the complete inhibition of L. panis PM1 cell growth, along with a significant reduction in end-products typically found during anaerobic growth. In silico analysis revealed that L. panis possessed two genes for NADH oxidase and NADH peroxidase, but their expression levels were not significantly affected by the presence of oxygen. Specific activities for these two enzymes were observed in crude extracts from L. panis PM1. Enzyme assays demonstrated that the majority of the H2O2 in the culture media was the product of NADH: H2O2 oxidase which was constitutively-active under both aerobic and microaerobic conditions; whereas, NADH peroxidase was positively-activated by the presence of oxygen and had a long induction time in contrast to NADH oxidase. These observations indicated that a coupled NADH oxidase - NADH peroxidase system was the main oxidative stress resistance mechanism in L. panis PM1, and was regulated by oxygen availability. Under aerobic conditions, NADH is mainly reoxidized by the NADH oxidase - peroxidase system rather than through the production of ethanol (or 1,3-propanediol or succinic acid production if glycerol or citric acid is available). This system helped L. panis PM1 directly use oxygen in its energy metabolism by producing extra ATP in contrast to homofermentative lactobacilli.

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  • The shift from fermentative to respiratory metabolism in lactic acid bacteria triggers early entrance into stationary phase and reroutes pyruvate away from lactate or lactate and ethanol, resulting in acetate accumulation.

    “The shift from fermentative to respiratory metabolism triggers in LAB an early entrance into the stationary phase along with marked changes in final products profiles, rerouting pyruvate away from lactate or from lactate and ethanol, respectively, in homofermentative and heterofermentative lactobacilli, resulting in acetate accumulation [46][47][48].”
  • Oxygen influences lactic acid bacteria metabolism, and air infiltration results in decline of lactic acid concentration in maize silage and barley silage.

    “However, oxygen influences LAB metabolism [46][47][48], and similar to our findings, other studies have reported that air infiltration results in the decline of lactic acid concentration in maize silage [10,11,13] and also in barley silage [12].”
  • Lactic acid bacteria are generally considered oxygen-tolerant anaerobes with a fermentative metabolism, and most can grow under aerobic conditions.

    “LAB are generally considered oxygen-tolerant anaerobes with a fermentative metabolism, meaning that most of them can grow under aerobic conditions [46].”

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Authors
Kang, T. S., Korber, D. R., & Tanaka, T.
Affiliations
University of Saskatchewan (CA)
Corresponding author
Tanaka, Takuji
Venue
AMB Express
Published
2013-01-31
Volume
3
Issue
1
Pages
10-10
ISSN
2191-0855 (ISSN-L)
OpenAlex
W2137514969
Cited by
55
References
24
Citations by year
2026: 6 · 2025: 5 · 2024: 1 · 2023: 4 · 2022: 5 · 2021: 3 · 2020: 9 · 2019: 2 · 2018: 3 · 2017: 2 · 2015: 3 · 2014: 7 · 2013: 5
FWCI
2.24
Type
journal article
Language
en
Open access
Licence
cc-by
Locations
  • AMB Express (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
Funders
  • Ministry of Agriculture - Saskatchewan
  • Agriculture and Agri-Food Canada
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Redox biology and oxidative stress
  • Life Sciences › Agricultural and Biological Sciences › Food Science › Probiotics and Fermented Foods
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
Keywords
NADH regeneration, oxidative stress resistance, NADH oxidase, NADH peroxidase, hydrogen peroxide, oxygen availability, aerobic growth, microaerobic growth, 1,3-propanediol, heterofermentative metabolism, energy metabolism, gene expression regulation

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