Aerobic metabolism in the genus Lactobacillus: impact on stress response and potential applications in the food industry
Abstract
This review outlines the recent advances in the knowledge on aerobic and respiratory growth of lactic acid bacteria, focusing on the features of respiration-competent lactobacilli. The species of the genus Lactobacillus have been traditionally classified as oxygen-tolerant anaerobes, but it has been demonstrated that several strains are able to use oxygen as a substrate in reactions mediated by flavin oxidases and, in some cases, to synthesize a minimal respiratory chain. The occurrence of genes related to aerobic and respiratory metabolism and to oxidative stress response apparently correlates with the taxonomic position of lactobacilli. Members of the ecologically versatile Lactobacillus casei, L. plantarum and L. sakei groups are apparently best equipped to deal with aerobic/respiratory growth. The shift from anaerobic growth to aerobic (oxygen) and/or respiratory promoting (oxygen, exogenous haem and menaquinone) conditions offers physiological advantages and affects the pattern of metabolite production in several species. Even if this does not result in dramatic increases in biomass production and growth rate, cells grown in these conditions have improved tolerance to heat and oxidative stresses. An overview of benefits and of the potential applications of Lactobacillus cultures grown under aerobic or respiratory conditions is also discussed.
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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].”
From The Effects of Short-Time Delayed Sealing on Fermentation, Aerobic Stability and Chemical Composition on Maize Silages (2023) · cites this paper as [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].”
From The Effects of Short-Time Delayed Sealing on Fermentation, Aerobic Stability and Chemical Composition on Maize Silages (2023) · cites this paper as [48]
Cites
Gänzle, M. G. (2015) · Current Opinion in Food Science · doi:10.1016/j.cofs.2015.03.001 · Cited by 936 · see citing works
Food fermentations: Microorganisms with technological beneficial use
Bourdichon, F., Casarégola, S., Farrokh, C., Frisvad, J. C., Gerds, M. L., Hammes, W. P., Harnett, J., Huys, G. R. B., Laulund, S., Ouwehand, A. C., et al. (2011) · International Journal of Food Microbiology · doi:10.1016/j.ijfoodmicro.2011.12.030 · Cited by 742 · see citing works
The cytochrome bd respiratory oxygen reductases
Borisov, V. B., Gennis, R. B., Hemp, J., & Verkhovsky, M. I. (2011) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/j.bbabio.2011.06.016 · Cited by 508 · see citing works
Chemistry and Reactions of Reactive Oxygen Species in Foods
Choe, E., & MIN, D. B. S. (2006) · Critical Reviews in Food Science and Nutrition · doi:10.1080/10408390500455474 · Cited by 346 · see citing works
Duwat, P., Sourice, S., Cesselin, B., Lamberet, G., Vido, K., Gaudu, P., Loir, Y. L., Violet, F., Loubière, P., & Gruss, A. (2001) · Journal of Bacteriology · doi:10.1128/jb.183.15.4509-4516.2001 · Cited by 245 · see citing works
Global control of sugar metabolism: a Gram-positive solution
Titgemeyer, F., & Hillen, W. (2002) · Antonie van Leeuwenhoek · doi:10.1023/a:1020628909429 · Cited by 238 · see citing works
Zheng, J., Ruan, L., Sun, M., & Gänzle, M. G. (2015) · Applied and Environmental Microbiology · doi:10.1128/aem.02116-15 · Cited by 236 · see citing works
Aerobic Respiration Metabolism in Lactic Acid Bacteria and Uses in Biotechnology
Pedersen, M. B., Gaudu, P., Lechardeur, D., Petit, M.-A., & Gruss, A. (2012) · Annual Review of Food Science and Technology · doi:10.1146/annurev-food-022811-101255 · Cited by 197 · see citing works
Heme and menaquinone induced electron transport in lactic acid bacteria
Brooijmans, R. J. W., Smit, B., dos Santos, F. B., van Riel, J., de Vos, W. M., & Hugenholtz, J. (2009) · Microbial Cell Factories · doi:10.1186/1475-2859-8-28 · Cited by 133 · see citing works
Using heme as an energy boost for lactic acid bacteria
Lechardeur, D., Cesselin, B., Fernandez, A., Lamberet, G., Garrigues, C., Pedersen, M. B., Gaudu, P., & Gruss, A. (2011) · Current Opinion in Biotechnology · doi:10.1016/j.copbio.2010.12.001 · Cited by 127 · see citing works
Current status and emerging role of glutathione in food grade lactic acid bacteria
Pophaly, S. D., Singh, R., Pophaly, S. D., et al. (2012) · Microbial Cell Factories · doi:10.1186/1475-2859-11-114 · Cited by 121 · see citing works
Rezaı̈ki, L., Cesselin, B., Yamamoto, Y., Vido, K., West, E. V., Gaudu, P., & Gruss, A. (2004) · Molecular Microbiology · doi:10.1111/j.1365-2958.2004.04217.x · Cited by 116 · see citing works
Kleerebezemab, M., Pascal Hols, A., & Hugenholtz, J. (2000) · Enzyme and Microbial Technology · doi:10.1016/s0141-0229(00)00180-0 · Cited by 110 · 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
Lorquet, F., Goffin, P., Muscariello, L., Baudry, J.-B., Ladero, V., Sacco, M., Kleerebezem, M., & Pascal Hols, A. (2004) · Journal of Bacteriology · doi:10.1128/jb.186.12.3749-3759.2004 · Cited by 103 · see citing works
<i>Lactobacillus plantarum</i> WCFS1 Electron Transport Chains
Brooijmans, R. J. W., de Vos, W. M., & Hugenholtz, J. (2009) · Applied and Environmental Microbiology · doi:10.1128/aem.00147-09 · Cited by 103 · see citing works
Pedersen, M. B., Garrigues, C., Tuphile, K., Brun, C., Vido, K., Bennedsen, M., Møllgaard, H., Gaudu, P., & Gruss, A. (2008) · Journal of Bacteriology · doi:10.1128/jb.00447-08 · Cited by 103 · see citing works
Rochat, T., Gratadoux, J., Gruss, A., Corthier, G., Maguin, E., Langella, P., & van de Guchte, M. (2006) · Applied and Environmental Microbiology · doi:10.1128/aem.00482-06 · Cited by 97 · see citing works
Pedersen, M. B., Iversen, S. L., Sørensen, K. I., & Johansen, E. (2005) · FEMS Microbiology Reviews · doi:10.1016/j.fmrre.2005.04.001 · Cited by 96 · see citing works
CcpA regulation of aerobic and respiration growth in Lactococcus lactis
Gaudu, P., Lamberet, G., Poncet, S., & Gruss, A. (2003) · Molecular Microbiology · doi:10.1046/j.1365-2958.2003.03700.x · Cited by 94 · see citing works
Serata, M., Iino, T., Yasuda, E., & Sako, T. (2012) · Microbiology · doi:10.1099/mic.0.053942-0 · Cited by 93 · 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
Self-citationZotta, T., Ricciardi, A., Guidone, A., Sacco, M., Muscariello, L., Mazzeo, M. F., Cacace, G., & Parente, E. (2012) · International Journal of Food Microbiology · doi:10.1016/j.ijfoodmicro.2012.01.017 · Cited by 88 · see citing works
Self-citationPot, B., Felis, G. E., Bruyne, K. D., Tsakalidou, E., Papadimitriou, K., Leisner, J. J., & Vandamme, P. A. R. (2014) · Wiley eBooks · doi:10.1002/9781118655252.ch19 · Cited by 83 · see citing works
Goffin, P., Lorquet, F., Kleerebezem, M., & Pascal Hols, A. (2004) · Journal of Bacteriology · doi:10.1128/jb.186.19.6661-6666.2004 · Cited by 82 · see citing works
Goffin, P., Muscariello, L., Lorquet, F., Stukkens, A., Prozzi, D., Sacco, M., Kleerebezem, M., & Pascal Hols, A. (2006) · Applied and Environmental Microbiology · doi:10.1128/aem.00659-06 · Cited by 78 · see citing works
Quatravaux, S., Remize, F., Bryckaert, É., Colavizza, D., & Guzzo, J. (2006) · Journal of Applied Microbiology · doi:10.1111/j.1365-2672.2006.02955.x · Cited by 77 · see citing works
de LeBlanc, A. D. M., del Carmen, S., Chatel, J., Miyoshi, A., Azevedo, V., Langella, P., Bermúdez‐Humarán, L. G., & LeBlanc, J. G. (2015) · Gastroenterology Research and Practice · doi:10.1155/2015/146972 · Cited by 72 · see citing works
Effect of respiration and manganese on oxidative stress resistance of Lactobacillus plantarum WCFS1
Watanabe, M., van der Veen, S., Nakajima, H., & Abee, T. (2011) · Microbiology · doi:10.1099/mic.0.051250-0 · Cited by 67 · see citing works
Diacetyl and acetoin production from whey permeate using engineered Lactobacillus casei
Nadal, I., Rico, J. J. R., Pérez‐Martínez, G., et al. (2009) · Journal of Industrial Microbiology & Biotechnology · doi:10.1007/s10295-009-0617-9 · Cited by 56 · see citing works
Stevens, M. J. A., Wiersma, A., de Vos, W. M., Kuipers, O. P., Smid, E. J., Douwe Molenaar, B., & Kleerebezem, M. (2008) · Applied and Environmental Microbiology · doi:10.1128/aem.00136-08 · Cited by 56 · see citing works
Kang, T. S., Korber, D. R., & Tanaka, T. (2013) · AMB Express · doi:10.1186/2191-0855-3-10 · Cited by 55 · see citing works
Bron, P. A., Wels, M., Bongers, R. S., de Veen, H. V. B., Wiersma, A., Overmars, L., Marco, M. L., & Kleerebezem, M. (2012) · PLoS ONE · doi:10.1371/journal.pone.0038720 · Cited by 54 · see citing works
Aerobic metabolism and oxidative stress tolerance in the Lactobacillus plantarum group
Guidone, A., Ianniello, R. G., Ricciardi, A., Zotta, T., & Parente, E. (2013) · World Journal of Microbiology and Biotechnology · doi:10.1007/s11274-013-1334-0 · Cited by 52 · see citing works
Self-citationLandete, J. M., Ferrer, S., Monedero, V., et al. (2013) · Applied and Environmental Microbiology · doi:10.1128/aem.01177-13 · Cited by 52 · 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
Self-citationJänsch, 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
Ianniello, R. G., Zotta, T., Matera, A., Genovese, F., Parente, E., & Ricciardi, A. (2016) · PLoS ONE · doi:10.1371/journal.pone.0164065 · Cited by 48 · see citing works
Self-citationAbriouel, H., Herrmann, A., Stärke, J., Yousif, N. M. K., Wijaya, A., Tauscher, B., Holzapfel, W. H., & Franz, C. M. A. P. (2004) · Applied and Environmental Microbiology · doi:10.1128/aem.70.1.603-606.2004 · Cited by 47 · see citing works
Mazzeo, M. F., Cacace, G., Peluso, A., et al. (2012) · Journal of Proteomics · doi:10.1016/j.jprot.2012.05.019 · Cited by 42 · see citing works
Reale, A., Ianniello, R. G., Ciocia, F., Renzo, T. D., Boscaino, F., Ricciardi, A., Coppola, R., Parente, E., Zotta, T., & McSweeney, P. L. H. (2016) · International Dairy Journal · doi:10.1016/j.idairyj.2016.08.005 · Cited by 41 · see citing works
Self-citationEffect of respirative cultures of Lactobacillus casei on model sourdough fermentation
Reale, A., Renzo, T. D., Zotta, T., Preziuso, M., Boscaino, F., Ianniello, R. G., Storti, L. V., Tremonte, P., & Coppola, R. (2016) · LWT · doi:10.1016/j.lwt.2016.06.065 · Cited by 38 · see citing works
Self-citationIanniello, 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
Self-citationIanniello, 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
Self-citationPudlik, A. M., & Lolkema, J. S. (2010) · Journal of Bacteriology · doi:10.1128/jb.01171-10 · Cited by 32 · 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
Joubert, L., Derré‐Bobillot, A., Gaudu, P., Gruss, A., & Lechardeur, D. (2014) · Molecular Microbiology · doi:10.1111/mmi.12705 · Cited by 32 · see citing works
de Felipe, F. L., & Gaudu, P. (2009) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-009-1897-8 · Cited by 31 · see citing works
Impact of Respiration on Resistance of Lactobacillus plantarum WCFS1 to Acid Stress
Watanabe, M., van der Veen, S., & Abee, T. (2012) · Applied and Environmental Microbiology · doi:10.1128/aem.00287-12 · Cited by 28 · see citing works
Eikmeyer, F., Heinl, S., Marx, H., Pühler, A., Grabherr, R. M., & Schlüter, A. (2015) · PLoS ONE · doi:10.1371/journal.pone.0134149 · Cited by 25 · see citing works
Wang, G., Yin, S., An, H., Chen, S., & Hao, Y. (2010) · Journal of Industrial Microbiology & Biotechnology · doi:10.1007/s10295-010-0871-x · Cited by 25 · see citing works
Li, C., Sun, J. W., Zhang, G. F., et al. (2015) · Journal of Dairy Science · doi:10.3168/jds.2015-10321 · Cited by 24 · see citing works
Aeration and fermentation strategies on nisin production
Jiang, L., Liu, Y., Yan, G., et al. (2015) · Biotechnology Letters · doi:10.1007/s10529-015-1886-1 · Cited by 23 · see citing works
Oxygen Relieves the CO2 and Acetate Dependency of Lactobacillus johnsonii NCC 533
Hertzberger, R. Y., Pridmore, R. D., Gysler, C., Kleerebezem, M., & de Mattos, M. J. T. (2013) · PLoS ONE · doi:10.1371/journal.pone.0057235 · Cited by 21 · see citing works
Larsen, N., Moslehi‐Jenabian, S., Werner, B. B., Jensen, M. L., Garrigues, C., Vogensen, F. K., & Jespersen, L. (2016) · International Journal of Food Microbiology · doi:10.1016/j.ijfoodmicro.2016.03.002 · Cited by 21 · see citing works
Regulation of EPS production in Lactobacillus casei LC2W through metabolic engineering
Li, N., Huang, Y., Liu, Z., You, C., & Guo, B. (2015) · Letters in Applied Microbiology · doi:10.1111/lam.12492 · Cited by 20 · see citing works
Liu, J., Wang, Q., Zou, H., et al. (2013) · Microbial Biotechnology · doi:10.1111/1751-7915.12046 · Cited by 17 · see citing works
Ge, X., Xu, Y. B., Chen, X., et al. (2015) · Journal of Microbiology and Biotechnology · doi:10.4014/jmb.1407.07001 · Cited by 16 · see citing works
Liu, Q., Hang, X., Liu, X., et al. (2011) · Annals of Microbiology · doi:10.1007/s13213-011-0237-2 · Cited by 14 · see citing works
Zotta, T., Tabanelli, G., Montanari, C., Ianniello, R. G., Parente, E., Gardini, F., & Ricciardi, A. (2016) · Journal of Applied Microbiology · doi:10.1111/jam.13373 · Cited by 13 · see citing works
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Maresca, D., Zotta, T., & Mauriello, G. (2018) · Frontiers in Microbiology · doi:10.3389/fmicb.2018.00157 · Cited by 66 · see citing works
Son, Y. S., Ki, S. J., Thanavel, R., Kim, J., Lee, M., Kim, J., Jung, C., Han, T., Cho, H., Ryu, C., et al. (2020) · The FASEB Journal · doi:10.1096/fj.202000063r · Cited by 45 · 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
Kim, S.-H., Singh, D., Kim, S.-A., Kwak, M. J., Cho, D., Kim, J., Roh, J.-H., Kim, W.-G., Han, N. S., & Lee, C. H. (2023) · Food Microbiology · doi:10.1016/j.fm.2023.104364 · Cited by 12 · see citing works
- Authors
- Zotta, T., Parente, E., & Ricciardi, A.
- Affiliations
- Institute of Food Science (IT)
- University of Basilicata (IT)
- Corresponding author
- Zotta, T.
- Venue
- Journal of Applied Microbiology
- Publisher
- Oxford University Press (OUP)
- Published
- 2017-02-16
- Volume
- 122
- Issue
- 4
- Pages
- 857-869
- ISSN
- 1364-5072 (ISSN-L)
- OpenAlex
- W2569232816
- Cited by
- 202
- References
- 60
- Citations by year
- 2026: 19 · 2025: 27 · 2024: 31 · 2023: 25 · 2022: 24 · 2021: 34 · 2020: 17 · 2019: 12 · 2018: 8 · 2017: 5
- FWCI
- 1.25
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Journal of Applied Microbiology (publishedVersion)
- PubMed (publishedVersion)
- CINECA IRIS Institutional Research Information System (University of Basilicata) (submittedVersion)
- Topics
- Life Sciences › Agricultural and Biological Sciences › Food Science › Probiotics and Fermented Foods
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Microbial metabolism and enzyme function
- Keywords
- Lactobacillus, aerobic metabolism, respiratory growth, oxidative stress response, heat tolerance, Lactobacillus casei, Lactobacillus plantarum, Lactobacillus sakei, vitamin K2, lactic acid bacteria, food industry applications
- MeSH terms
- Aerobiosis, Industrial Microbiology, Lactobacillus, Oxygen, Oxidative Stress, Food Industry
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