Influence of Oxygen on NADH Recycling and Oxidative Stress Resistance Systems in Lactobacillus panis PM1
Open accessAbstract
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.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
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].”
From The Effects of Short-Time Delayed Sealing on Fermentation, Aerobic Stability and Chemical Composition on Maize Silages (2023) · cites this paper as [46]
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].”
From The Effects of Short-Time Delayed Sealing on Fermentation, Aerobic Stability and Chemical Composition on Maize Silages (2023) · cites this paper as [46]
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].”
From The Effects of Short-Time Delayed Sealing on Fermentation, Aerobic Stability and Chemical Composition on Maize Silages (2023) · cites this paper as [46]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Analysis of Relative Gene Expression Data Using Real-Time Quantitative PCR and the 2−ΔΔCT Method
Livak, K. J., & Schmittgen, T. D. (2001) · Methods · doi:10.1006/meth.2001.1262 · Cited by 180,860 · see citing works
Isolation and characterization
Turksen, K. (2006) · Humana Press eBooks · Cited by 2,082 · see citing works
Oxidative stress responses in Escherichia coli and Salmonella typhimurium
Farr, S. B., & Kogoma, T. (1991) · Microbiological Reviews · doi:10.1128/mr.55.4.561-585.1991 · Cited by 1,091 · see citing works
Carbohydrate metabolism in lactic acid bacteria
Kandler, O. (1983) · Antonie van Leeuwenhoek · doi:10.1007/bf00399499 · Cited by 901 · see citing works
Microbial production of 1,3-propanediol: Recent developments and emerging opportunities
Saxena, R. K., Anand, P., Saran, S., & Isar, J. (2009) · Biotechnology Advances · doi:10.1016/j.biotechadv.2009.07.003 · Cited by 486 · see citing works
Responses of lactic acid bacteria to oxygen
Condon, S. (1987) · FEMS Microbiology Letters · doi:10.1111/j.1574-6968.1987.tb02465.x · Cited by 417 · see citing works
Talarico, T. L., Axelsson, L. T., Novotny, J. F., Fiuzat, M., & Dobrogosz, W. J. (1990) · Applied and Environmental Microbiology · doi:10.1128/aem.56.4.943-948.1990 · Cited by 148 · see citing works
Marty-Teysset, C., de la Torre, F., & Garel, J. R. (2000) · Applied and Environmental Microbiology · doi:10.1128/aem.66.1.262-267.2000 · Cited by 143 · see citing works
Effect of glucose on glycerol bioconversion by Lactobacillus reuteri
thi-Peng, Q. L. X. F., Dileme, F., & Puhan, Z. (2002) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-002-1002-z · Cited by 124 · see citing works
Oxidative stress in Lactococcus lactis.
Miyoshi, A., Rochat, T., Gratadoux, J., Loir, Y. L., Oliveira, S. C., Langella, P., & Azevedo, V. (2003) · PubMed · Cited by 122 · see citing works
Purification and biochemical characterization of pyruvate oxidase from Lactobacillus plantarum
Sedewitz, B., Schleifer, K. H., & Götz, F. (1984) · Journal of Bacteriology · doi:10.1128/jb.160.1.273-278.1984 · Cited by 108 · see citing works
Pedersen, C., Jonsson, H., Lindberg, J. E., & Roos, S. (2004) · Applied and Environmental Microbiology · doi:10.1128/aem.70.3.1522-1527.2004 · Cited by 108 · see citing works
Higuchi, M., Yamamoto, Y., & Kamio, Y. (2000) · Journal of Bioscience and Bioengineering · doi:10.1016/s1389-1723(01)80028-1 · Cited by 107 · see citing works
Formation of Hydrogen Peroxide by Group N Streptococci and Its Effect on Their Growth and Metabolism
Anders, R. F., Hogg, D. M., & Jago, G. R. (1970) · Applied Microbiology · doi:10.1128/am.19.4.608-612.1970 · Cited by 104 · see citing works
Aerobic growth of and activities of NADH oxidase and NADH peroxidase in lactic acid bacteria
Sakamoto, M., & Komagata, K. (1996) · Journal of Fermentation and Bioengineering · doi:10.1016/0922-338x(96)88810-6 · Cited by 92 · see citing works
McFeeters, R. F., & Chen, K.-H. (1986) · Food Microbiology · doi:10.1016/s0740-0020(86)80029-6 · Cited by 68 · see citing works
An, H., Zhai, Z., Yin, S., Luo, Y., Han, B., & Hao, Y. (2011) · Journal of Agricultural and Food Chemistry · doi:10.1021/jf200251k · Cited by 64 · see citing works
1,3-Propanediol:NAD+ oxidoreductases of Lactobacillus brevis and Lactobacillus buchneri
Veiga‐da‐Cunha, M., & Foster, M. A. (1992) · Applied and Environmental Microbiology · doi:10.1128/aem.58.6.2005-2010.1992 · Cited by 51 · see citing works
Jänsch, A., Freiding, S., Behr, J., & Vogel, R. F. (2010) · Food Microbiology · doi:10.1016/j.fm.2010.08.001 · Cited by 48 · see citing works
An, H., Zhou, H., Huang, Y., Wang, G., Luan, C., Mou, J., Luo, Y., & Hao, Y. (2010) · Molecular Biotechnology · doi:10.1007/s12033-010-9254-9 · Cited by 46 · see citing works
A rapid method for RNA preparation from Gram-positive bacteria
Oh, E. T., & So, J.-S. (2003) · Journal of Microbiological Methods · doi:10.1016/s0167-7012(02)00218-x · Cited by 42 · see citing works
Khan, N. H., Kang, T. S., Grahame, D. A. S., Haakensen, M. C., Ratanapariyanuch, K., Reaney, M. J. T., Korber, D. R., & Tanaka, T. (2012) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-012-4386-4 · Cited by 41 · see citing works
Tachon, S., Chambellon, É., & Yvon, M. (2011) · Journal of Bacteriology · doi:10.1128/jb.01466-10 · Cited by 20 · see citing works
Chen, K.-H., & McFeeters, R. F. (1986) · Food Microbiology · doi:10.1016/s0740-0020(86)80030-2 · Cited by 17 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Feng, T., & Wang, J. (2020) · Gut microbes · doi:10.1080/19490976.2020.1801944 · Cited by 574 · see citing works
Zotta, T., Parente, E., & Ricciardi, A. (2017) · Journal of Applied Microbiology · doi:10.1111/jam.13399 · Cited by 202 · see citing works
Fructophilic Lactic Acid Bacteria, a Unique Group of Fructose-Fermenting Microbes
Endo, A., Maeno, S., Tanizawa, Y., Kneifel, W., Arita, M., Dicks, L. M. T., & Salminen, S. (2018) · Applied and Environmental Microbiology · doi:10.1128/aem.01290-18 · Cited by 156 · see citing works
Assessment of Aerobic and Respiratory Growth in the Lactobacillus casei Group
Zotta, T., Ricciardi, A., Ianniello, R. G., Parente, E., Reale, A., Rossi, F., Iacumin, L., Comi, G., & Coppola, R. (2014) · PLoS ONE · doi:10.1371/journal.pone.0099189 · Cited by 92 · see citing works
Antioxidant Properties of Lactic Acid Bacteria
Bryukhanov, A. L., Klimko, A. I., & Netrusov, A. I. (2022) · Microbiology · doi:10.1134/s0026261722601439 · Cited by 91 · see citing works
Atomically dispersed N-coordinated Fe-Fe dual-sites with enhanced enzyme-like activities
Jiao, L., Ye, W., Kang, Y., Zhang, Y., Xu, W., Wu, Y., Gu, W., Song, W., Xiong, Y., & Zhu, C. (2021) · Nano Research · doi:10.1007/s12274-021-3581-y · Cited by 77 · see citing works
Lin, X., Xia, Y., Yang, Y., Wang, G., Zhou, W., & Ai, L. (2020) · LWT · doi:10.1016/j.lwt.2020.109278 · Cited by 70 · see citing works
Adaptation to Aerobic Environment of Lactobacillus johnsonii/gasseri Strains
Maresca, D., Zotta, T., & Mauriello, G. (2018) · Frontiers in Microbiology · doi:10.3389/fmicb.2018.00157 · Cited by 66 · see citing works
Pathogen control at the intestinal mucosa – H2O2to the rescue
Knaus, U. G., Hertzberger, R. Y., Pîrcălăbioru, G. G., Yousefi, S. P. M., & dos Santos, F. B. (2017) · Gut Microbes · doi:10.1080/19490976.2017.1279378 · Cited by 58 · see citing works
Aerobic and respirative growth of heterofermentative lactic acid bacteria: A screening study
Zotta, T., Ricciardi, A., Ianniello, R. G., Storti, L. V., Glibota, N., & Parente, E. (2018) · Food Microbiology · doi:10.1016/j.fm.2018.02.017 · Cited by 55 · see citing works
Gao, Y., Liu, Y., Sun, M., Zhang, H., Mu, G., & Tuo, Y. (2020) · Journal of Dairy Science · doi:10.3168/jds.2019-18047 · Cited by 51 · see citing works
Nano iron materials enhance food waste fermentation
Wang, Q., Feng, K. M., & Li, H. (2020) · Bioresource Technology · doi:10.1016/j.biortech.2020.123804 · Cited by 51 · see citing works
Temperature and respiration affect the growth and stress resistance of Lactobacillus plantarum C17
Zotta, T., Guidone, A., Ianniello, R. G., Parente, E., & Ricciardi, A. (2013) · Journal of Applied Microbiology · doi:10.1111/jam.12285 · Cited by 50 · see citing works
Fokum, E., Zabed, H. M., Yun, J., Zhang, G., & Qi, X. (2021) · International Journal of Environmental Science and Technology · doi:10.1007/s13762-020-03036-w · Cited by 47 · see citing works
The Possible Role of Probiotic Supplementation in Inflammation: A Narrative Review
Colletti, A., Pellizzato, M., & Cicero, A. F. G. (2023) · Microorganisms · doi:10.3390/microorganisms11092160 · Cited by 44 · see citing works
Arcanjo, N. M. D. O., Andrade, M. J., Padilla, P., Rodríguez, A., Madruga, M. S., & Estévez, M. (2019) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2019.02.023 · Cited by 40 · see citing works
Gao, Y., Liang, Q., Sun, J., Wu, X., Song, Y., Xu, Y., Nie, H., HUANG, J. C., & Mu, G. (2025) · Food Bioscience · doi:10.1016/j.fbio.2025.106181 · Cited by 39 · see citing works
Ianniello, R. G., Ricciardi, A., Parente, E., Tramutola, A., Reale, A., & Zotta, T. (2014) · LWT · doi:10.1016/j.lwt.2014.10.020 · Cited by 37 · see citing works
Yildiz, S., Bonifacio, J. P. P., Bergé, M., González‐Ruiz, V., Baud, D., Kloehn, J., Boal‐Carvalho, I., Schären, O. P., Schotsaert, M., Hathaway, L. J., et al. (2020) · eLife · doi:10.7554/elife.53581 · Cited by 40 · see citing works
Ianniello, R. G., Zheng, J., Zotta, T., Ricciardi, A., & Gänzle, M. G. (2015) · Journal of Applied Microbiology · doi:10.1111/jam.12853 · Cited by 33 · see citing works
Kang, T. S., Korber, D. R., & Tanaka, T. (2013) · Applied and Environmental Microbiology · doi:10.1128/aem.02377-13 · Cited by 33 · see citing works
Kang, T. S., Korber, D. R., & Tanaka, T. (2013) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-013-5108-2 · Cited by 32 · see citing works
Antioxidant Mechanism of Lactiplantibacillus plantarum KM1 Under H2O2 Stress by Proteomics Analysis
Tian, Y., Wang, Y., Zhang, N., Xiao, M., Zhang, J., Xing, X., Zhang, Y., Fan, Y., Li, X., Nan, B., et al. (2022) · Frontiers in Microbiology · doi:10.3389/fmicb.2022.897387 · Cited by 30 · see citing works
Vieira, P. B., Kilikian, B. V., Bastos, R. V., Perpetuo, E. A., & do Nascimento, C. A. O. (2014) · Biochemical Engineering Journal · doi:10.1016/j.bej.2014.11.003 · Cited by 28 · see citing works
Kang, T. S., Korber, D. R., & Tanaka, T. (2014) · Applied and Environmental Microbiology · doi:10.1128/aem.01454-14 · Cited by 22 · see citing works
Antibacterial Activity and Prebiotic Properties of Six Types of Lamiaceae Honey
Nazzaro, F., Ombra, M. N., Coppola, F., Giulio, B. D., d’Acierno, A., Coppola, R., & Fratianni, F. (2024) · Antibiotics · doi:10.3390/antibiotics13090868 · Cited by 22 · see citing works
Gao, Y., Liu, Y., Ma, F., Sun, M., Mu, G., & Tuo, Y. (2020) · Journal of Proteomics · doi:10.1016/j.jprot.2020.103903 · Cited by 20 · see citing works
Kang, T. S., Korber, D. R., & Tanaka, T. (2013) · Journal of Applied Microbiology · doi:10.1111/jam.12291 · Cited by 20 · see citing works
Xia, Y., Gong, Y., Lin, X., Yang, Y., Song, X., Wang, G., Xiong, Z., Qian, Y., Liao, Z., Zhang, H., et al. (2023) · Food Science and Human Wellness · doi:10.26599/fshw.2022.9250076 · Cited by 19 · see citing works
A genomic view on lactic metabolism
Qiao, N., & Gänzle, M. G. (2025) · Food Microbiology · doi:10.1016/j.fm.2025.104945 · Cited by 18 · see citing works
Li, H., Chen, C., Li, Y., Li, Z., Li, C., & Luan, C. (2023) · Foods · doi:10.3390/foods12234276 · Cited by 19 · see citing works
Evaluation and mechanism of the antioxidant activity of lactic acid bacteria
Xiao, Y., Yang, J., Zhang, X., Meng, Y., Qin, Y., Huang, P., & Liu, D. (2025) · Folia Microbiologica · doi:10.1007/s12223-025-01277-1 · Cited by 18 · see citing works
Role of Plasmids in Beer Spoilage Lactic Acid Bacteria: A Review
Suzuki, K., Shinohara, Y., & Kurniawan, Y. N. (2020) · Journal of the American Society of Brewing Chemists · doi:10.1080/03610470.2020.1843899 · Cited by 16 · see citing works
Valladares, R. B., Graves, C. L., Wright, K., Gardner, C. L., Lorca, G. L., & González, C. F. (2015) · Frontiers in Microbiology · doi:10.3389/fmicb.2015.00716 · Cited by 16 · see citing works
de Melo, N. N., Carvalho-Estrada, P. D. A., Tavares, Q. G., Pereira, L. D. M., Delai Vigne, G. L., Camargo Rezende, D. M. L., & Schmidt, P. (2023) · Agronomy · doi:10.3390/agronomy13010223 · Cited by 15 · see citing works
Hagi, T., Kobayashi, M., & Nomura, M. (2015) · FEMS Microbiology Letters · doi:10.1093/femsle/fnv075 · Cited by 15 · see citing works
Ricciardi, A., Storti, L. V., Giavalisco, M., Parente, E., & Zotta, T. (2022) · Foods · doi:10.3390/foods11040535 · Cited by 14 · see citing works
Meng, Y., Liang, Z., Yi, M., Tan, Y. C., Li, Z., Du, P., Li, A., Li, C., & Liu, L. (2021) · LWT · doi:10.1016/j.lwt.2021.112462 · Cited by 13 · see citing works
Park, J. C., Kim, Y., & Lee, H.-S. (2014) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-014-6327-x · Cited by 10 · see citing works
Liu, Q., Yin, G., & Zhang, J. (2020) · Biological Control · doi:10.1016/j.biocontrol.2020.104318 · Cited by 8 · see citing works
Abrashev, R., Krumova, E. T., Atanasova, N., Dobreva, L. I., Angelova, M., & Danova, S. T. (2026) · Foods · doi:10.3390/foods15071253 · Cited by 7 · see citing works
Peter, S. B., Qiao, Z., Godspower, H. N., Omedi, J. O., Zhang, X., Xu, M., & Rao, Z. (2022) · Systems Microbiology and Biomanufacturing · doi:10.1007/s43393-022-00126-3 · Cited by 6 · see citing works
Fermentation redox potential control on the 1,3-propanediol production by Lactobacillus panis PM1
Wu, Y., & Lin, Y. (2022) · Process Biochemistry · doi:10.1016/j.procbio.2022.01.020 · Cited by 4 · see citing works
Ampemohotti, T., Spooner, C., Eastwood, S., Golneshin, A., Brennan, C. S., Pillidge, C. J., & Van, T. T. H. (2025) · Foods · doi:10.3390/foods14193395 · Cited by 3 · see citing works
Maresca, D., Filippis, F. D., Robertiello, A., & Mauriello, G. (2019) · Microorganisms · doi:10.3390/microorganisms7070200 · Cited by 2 · see citing works
Kang, T. S., Korber, D. R., & Tanaka, T. (2014) · Biotechnology Letters · doi:10.1007/s10529-014-1477-6 · Cited by 3 · see citing works
Electro-Fermentation Technology: Emerging Platform
Singh, M. P., Joshi, G., & Ali, M. A. (2020) · Springer eBooks · doi:10.1007/978-981-15-6872-5_4 · Cited by 2 · see citing works
Bedin, M. (2014) · Portuguese National Funding Agency for Science, Research and Technology (RCAAP Project by FCT)
Proteomic Analysis of the Levilactobacillus brevis 47f Strain under Oxidative Stress
Poluektova, E. U., Мавлетова, Д. А., Ziganshin, R., & Даниленко, В. Н. (2025) · Russian Journal of Genetics · doi:10.1134/s1022795424701655
Probiotics for managing non-alcoholic fatty liver disease: efficacy and mechanistic insights
Ghosh, S., Ghosh, A. J., Adhikari, M. D., Tiwary, B. K., & Saha, T. (2026) · Journal of Diabetes & Metabolic Disorders · doi:10.1007/s40200-026-01861-3
Huang, Z., Zhang, Y., Li, L., Gao, Y., Gu, Z., Cheng, L., & Hong, Y. (2026) · Food Chemistry · doi:10.1016/j.foodchem.2026.150826
Li, L., Zhang, J., Qu, S., Zhou, Z., Wang, B., Wu, H., Guo, Z., Shi, L., Yin, B., Zhu, X., et al. (2026) · Applied and Environmental Microbiology · doi:10.1128/aem.00954-26
Li, M., Mao, J., Liu, S., Yu, H., Qin, H., Liu, X., Tu, R., Chen, S., Liu, Z., Zhang, S., et al. (2026) · Gut Microbes · doi:10.1080/19490976.2026.2734657
- 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)
- PMC
- PMC3605185
- 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
- gold
- doi.org
- 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
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review