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Transcriptomic Analysis of the Levilactobacillus brevis 47f Strain under Oxidative Stress

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Abstract

Levilactobacillus brevis 47f is a heterofermentative aerotolerant lactic acid bacterium isolated from the microbiota of the gastrointestinal tract of a healthy human. Previously, the strain showed anti-inflammatory properties and protects the murine intestine from enteropathy induced by 5-fluorouracil as part of preclinical studies. At the same time, the molecular mechanisms that account for the properties of the strain and its response to the action of reactive oxygen species remain unexplored. The aim of this work is to study the response of the strain to the action of oxidizing agents (hydrogen peroxide and oxygen) using the transcriptional RNAseq analysis. Both oxidants exhibited a strong effect on the strain, increasing or decreasing the expression of several hundred genes: both general and specific for each oxidant. The characteristics of proteins whose expression was increased the most (DE ≥ 5) are provided. The genes activated under the action of both oxidants encode proteins related to stress, antioxidant activity, protein and nucleotide repair, cell wall, carbohydrate transport and metabolism, and catabolic energy-storage pathways. Peroxide mainly activates the transcription of defense proteins, namely, stress response and molecular chaperones, antioxidant activity, DNA repair, and proteins involved in the formation of the cell wall. Under aerobic conditions, the genes that encode proteins involved in energy conversion (the use of fatty acids, nucleosides, and fructose in addition to glucose as an energy source; proteins of the phosphoketolase pathway) and the import of peptides, amino acids, and sugars, are activated to a large extent. The data obtained in this work will be used by us to conduct an integrated analysis of transcriptomic, proteomic, and metabolomic data derived from this strain. This will make a significant contribution to the creation of a pharmabiotic based on L. brevis 47f for the treatment of various inflammatory diseases.

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REFERENCES

  1. Feyereisen, M., Mahony, J., Kelleher, P., et al., Comparative genome analysis of the Lactobacillus brevis species, BMC Genomics, 2019, vol. 20, no. 1, р. 416. https://doi.org/10.1186/s12864-019-5783-1

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Kim, K.T., Yang, S.J., and Paik, H.D., Probiotic properties of novel probiotic Levilactobacillus brevis KU15147 isolated from radish kimchi and its antioxidant and immune-enhancing activities, Food Sci. Biotechnol., 2021, vol. 30, pp. 257—265. https://doi.org/10.1007/s10068-020-00853-0

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Stankovic, M., Veljovic, K., Popovic, N., et al., Lactobacillus brevis BGZLS10-17 and Lb. plantarum BGPKM22 exhibit anti-inflammatory effect by attenuation of NF-κB and MAPK signaling in human bronchial epithelial cells, Int. J. Mol. Sci., 2022, vol. 23, no. 10, р. 5587. https://doi.org/10.3390/ijms23105547

    Article  CAS  Google Scholar 

  4. Kumar, S., Praneet, N.S., and Suchiang, K., Lactobacillus brevis MTCC 1750 enhances oxidative stress resistance and lifespan extension with improved physiological and functional capacity in Caenorhabditis elegans via the DAF-16 pathway, Free Radic. Res., 2022, vol. 56, nos. 7—8, pp. 555—571. https://doi.org/10.1080/10715762.2022.2155518

    Article  CAS  PubMed  Google Scholar 

  5. Danilenko, V.N., Devyatkin, A.V., Marsova, M.V., et al., Common inflammatory mechanisms in COVID-19 and Parkinson’s diseases: the role of microbiome and probiotics in their prevention, J. Inflamm. Res., 2021, vol. 14, pp. 6349—6381. https://doi.org/10.2147/JIR.S333887

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Yunes, R.A., Poluektova, E.U., Belkina, T.V., and Danilenko, V.N., Lactobacilli: legal regulation and prospects for new generation drugs, Appl. Biochem. Microbiol., 2022, vol. 58, pp. 652—664. https://doi.org/10.1134/S0003683822050179

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Sporer, A.J., Kahl, L.J., Price-Whelan, A., and Dietrich, L.E.P., Redox-based regulation of bacterial development and behavior, Ann. Rev. Biochem., 2017, vol. 86, pp. 777—797. https://doi.org/10.1146/annurev-biochem-061516-044453

    Article  CAS  PubMed  Google Scholar 

  8. Zotta, T., Parente, E., and Ricciardi, A., Aerobic metabolism in the genus Lactobacillus: impact on stress response and potential applications in the food industry, J. Appl. Microbiol., 2017, vol. 122, no. 4, pp. 857—869. https://doi.org/10.1111/jam.13399

    Article  CAS  PubMed  Google Scholar 

  9. Zotta, T., Ricciardi, A., Ianniello, R.G., et al., Aerobic and respirative growth of heterofermentative lactic acid bacteria: a screening study, Food Microbiol., 2018, vol. 76, pp. 117—127. https://doi.org/10.1016/j.fm.2018.02.017

    Article  CAS  PubMed  Google Scholar 

  10. Bryukhanov, A.L., Klimko, A.I., and Netrusov, A.I., Antioxidant properties of lactic acid bacteria, Microbio-logy (Moscow), 2022, vol. 91, pp. 463—478. https://doi.org/10.1134/S0026261722601439

    Article  CAS  Google Scholar 

  11. Yunes, R.A., Poluektova, E.U., Dyachkova, M.S., et al., GABA production and structure of gadB/gadC genes in Lactobacillus and Bifidobacterium strains from human microbiota, Anaerobe, 2016, vol. 42, pp. 197—204. https://doi.org/10.1016/j.anaerobe.2016.10.011

    Article  CAS  PubMed  Google Scholar 

  12. Marsova, M.V., Abilev, S.K., Poluektova, E.U., and Danilenko, V.N., A bioluminescent test system reveals valuable antioxidant properties of Lactobacillus strains from human microbiota, World J. Microbiol. Biotechnol., 2018, vol. 34, no. 2, p. 27. https://doi.org/10.1007/s11274-018-2410-2

    Article  CAS  PubMed  Google Scholar 

  13. Marsova, M., Odorskaya, M., Novichkova, M., et al., The Lactobacillus brevis 47f strain protects the murine intestine from enteropathy induced by 5-fluorouracil, Microorganisms, 2020, vol. 8, no. 6, р. 876. https://doi.org/10.3390/microorganisms8060876

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Olekhnovich, E.I., Batotsyrenova, E.G., Yunes, R.A., et al., The effects of Levilactobacillus brevis on the physiological parameters and gut microbiota composition of rats subjected to desynchronosis, Microb. Cell Fact., 2021, vol. 20, р. 226. https://doi.org/10.1186/s12934-021-01716-x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. DeMan, J.C., Rogosa, M., and Sharpe, M.E., A medium for the cultivation of lactobacilli, J. Appl. Microbiol., 1960, vol. 23, no. 1, pp. 130—135. https://doi.org/10.1111/j.1365-2672.1960.tb00188.x

    Article  Google Scholar 

  16. Bolger, A.M., Lohse, M., and Usadel, B., Trimmomatic: a flexible trimmer for Illumina sequence data, Bioinformatics, 2014, vol. 30, no. 15, pp. 2114—2120. https://doi.org/10.1093/bioinformatics/btu170

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Kim, D., Paggi, J.M., Park, C., et al., Graph-based genome alignment and genoty** with HISAT2 and HISAT‑genotype, Nat. Biotechnol., 2019, vol. 37, no. 8, pp. 907—915. https://doi.org/10.1038/s41587-019-0201-4

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Danecek, P., Bonfield, J.K., Liddle, J., et al., Twelve years of SAMtools and BCFtools, GigaScience, 2021, vol. 10, no. 2, р. giab008. https://doi.org/10.1093/gigascience/giab008

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Putri, G.H., Anders, S., Pyl, P.T., et al., Analysing high-throughput sequencing data in Python with HTSeq 2.0., Bioinformatics, 2022, р. btac166. https://doi.org/10.1093/bioinformatics/btac166

  20. Averina, O.V., Poluektova, E.U., Marsova, M.V., and Danilenko, V.N., Biomarkers and utility of the antioxidant potential of probiotic lactobacilli and bifidobacteria as representatives of the human gut microbiota, Biomedicines, 2021, vol. 9, no. 10, р. 1340.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Basu Thakur, P., Long, A.R., Nelson, B.J., et al., Complex responses to hydrogen peroxide and hypochlorous acid by the probiotic bacterium Lactobacillus reuteri, mSystems, 2019, vol. 4, no. 5, р. e00453-19. https://doi.org/10.1128/mSystems.00453-19

    Article  PubMed  PubMed Central  Google Scholar 

  22. Zhang, C., Gui, Y., Chen, X., et al., Transcriptional homogenization of Lactobacillus rhamnosus hsryfm 1301 under heat stress and oxidative stress, Appl. Microbiol. Biotechnol., 2020, vol. 104, no. 6, pp. 2611—2621. https://doi.org/10.1007/s00253-020-10407-3

    Article  CAS  PubMed  Google Scholar 

  23. Huang, R., Pan, M., Wan, C., et al., Physiological and transcriptional responses and cross protection of Lactobacillus plantarum ZDY2013 under acid stress, J. Dairy Sci., 2016, vol. 99, no. 2, pp. 1002—1010. https://doi.org/10.3168/jds.2015-9993

    Article  CAS  PubMed  Google Scholar 

  24. Zhang, C., Lu, J., Yang, D., et al., Stress influenced the aerotolerance of Lactobacillus rhamnosus hsryfm 1301, Biotechnol. Lett., 2018, vol. 40, pp. 729—735. https://doi.org/10.1007/s10529-018-2523-6

    Article  CAS  PubMed  Google Scholar 

  25. Kilstrup, M., Hammer, K., Jensen, P.R., and Martinussen, J., Nucleotide metabolism and its control in lactic acid bacteria, FEMS Microbiol. Rev., 2005, vol. 29, no. 3, pp. 555—590. https://doi.org/10.1016/j.femsre.2005.04.006

    Article  CAS  PubMed  Google Scholar 

  26. Tozzi, M.G., Camici, M., Mascia, L., et al., Pentose phosphates in nucleoside interconversion and catabolism, FEBS J., 2006, vol. 273, no. 6, pp. 1089—1101. https://doi.org/10.1111/j.1742-4658.2006.05155.x

    Article  CAS  PubMed  Google Scholar 

  27. De Carvalho, C.C.C.R. and Caramujo, M.J., The various roles of fatty acids, Molecules, 2018, vol. 23, no. 10, р. 2583. https://doi.org/10.3390/molecules231025832018

    Article  PubMed  PubMed Central  Google Scholar 

  28. Winkler, J. and Kao, K.C., Transcriptional analysis of Lactobacillus brevis to N-butanol and ferulic acid stress responses, PLoS One, 2011, vol. 6, no. 8, р. c21438. https://doi.org/10.1371/journal.pone.0021438

    Article  CAS  Google Scholar 

  29. Maresca, D., Zotta, T., and Mauriello, G., Adaptation to aerobic environment of Lactobacillus johnsonii/gasseri strains, Front. Microbiol., 2018, vol. 9, р. 157. https://doi.org/10.3389/fmicb.2018.00157

  30. Zhai, Z., Yang, Y., Wang, H., et al., Global transcriptomic analysis of Lactobacillus plantarum CAUH2 in response to hydrogen peroxide stress, Food Microbiol., 2020, vol. 87, р. 103389. https://doi.org/10.1016/j.fm.2019.103389

    Article  CAS  PubMed  Google Scholar 

  31. Poluektova, E.U., Mavletova, D.A., Odorskaya, M.V., et al., Comparative genomic, transcriptomic, and proteomic analysis of the Limosilactobacillus fermentum U-21 strain promising for the creation of a pharmabiotic, Russ. J. Genet., 2022, vol. 58, no. 9, pp. 1079—1090. https://doi.org/10.1134/S1022795422090125

    Article  CAS  Google Scholar 

  32. Stevens, M.J.A., Wiersma, A., de Vos, W.M., et al., Improvement of Lactobacillus plantarum aerobic growth as directed by comprehensive transcriptome analysis, Appl. Environ. Microbiol., 2008, vol. 74, no. 15, pp. 4776—4778. https://doi.org/10.1128/AEM.00136-08

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Eikmeyer, F.G., Heinl, S., Marx, H., et al., Identification of oxygen-responsive transcripts in the silage inoculant Lactobacillus buchneri CD034 by RNA sequencing, PLoS One, 2015, vol. 10, no. 7, р. 0134149. https://doi.org/10.1371/journal.pone.0134149

    Article  CAS  Google Scholar 

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Funding

The study was supported by the Russian Foundation for Basic Research, project no. 20-54-18006. The participation of V.N. Danilenko and E.U. Poluektova was also funded by State Task no. 0092-2022-0003.

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Correspondence to E. U. Poluektova.

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This article does not contain any studies involving animals or human participants performed by any of the authors.

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Translated by M. Novikova

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Poluektova, E.U., Averina, O.V., Kovtun, A.S. et al. Transcriptomic Analysis of the Levilactobacillus brevis 47f Strain under Oxidative Stress. Russ J Genet 59, 770–778 (2023). https://doi.org/10.1134/S1022795423080100

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