Cold induced expression of a novel levansucrase gene sacB1 enhances exopolysaccharide production and stress resilience in Leuconostoc mesenteroides

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Date
2025-07-02
Authors
Fernandez de Ullivarri, Miguel
Buttimer, Colin
Wijman, Janneke
Heintz, Eelco
Ross, Paul
McCusker, Matthew P.
Hill, Colin
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Nature Research
Published Version
10.1038/s41598-025-04141-x
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Abstract
Exopolysaccharides (EPS) play critical roles in microbial survival, stress adaptation, and biofilm formation across diverse environments. In food-associated bacteria such as Leuconostoc mesenteroides, understanding the regulation of EPS production under environmental stress is important for both spoilage control and industrial applications. However, the mechanisms linking cold stress to EPS biosynthesis remain poorly understood. Here, we show that sucrose and low temperature (8 °C) trigger a metabolic shift from dextran-only to combined dextran and levan biosynthesis in four meat-borne Leuc. mesenteroides strains. Two high EPS-producing strains (HEPRs) possess the sacB_1 gene, which encodes a previously uncharacterized levansucrase absent from low EPS-producing strains (LEPRs) that only carry the levS gene. This is the first study to describe the role of sacB_1 in cold-induced EPS production. Notably, sacB_1 was also identified in Leuc. mesenteroides strains isolated from plant-based fermentations such as kimchi and birch sap, but the HEPR strains analyzed here are the only known meat-derived isolates to carry this gene. Genomic analyses revealed highly conserved biosynthetic clusters for dextran, heteropolysaccharide, and levan. Gene expression profiling showed that levS and sacB_1 were upregulated at 8 °C, while dsrD expression was favoured at 25 °C. Cold-induced sucrose metabolism, characterized by high expression of levS, sacB_1, and dsrD, enhanced cell viability under oxidative stress. Furthermore, heterologous expression of sacB_1 in Leuc. mesenteroides and Lactococcus lactis improved resilience under cold and high-aeration conditions, confirming the protective role of levan. These findings advance the understanding of temperature-dependent EPS regulation in LAB and highlight sucrase diversity as a key factor in microbial adaptation to environmental stress.
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Keywords
Cold stress , Exopolysaccharide , Leuconostoc mesenteroides , Levansucrase , Sucrose-induced metabolism
Citation
Fernandez de Ullivarri, M., Buttimer, C., Wijman, J., Heintz, E., Ross, P., McCusker, M. P. and Hill, C. (2025) 'Cold induced expression of a novel levansucrase gene sacB1 enhances exopolysaccharide production and stress resilience in Leuconostoc mesenteroides', Scientific Reports, 15(1), 22980 (17pp). https://doi.org/10.1038/s41598-025-04141-x
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https://hdl.handle.net/10468/17721
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APC Microbiome Ireland - Journal Articles
Microbiology - Journal Articles
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© 2025, the Author(s). Open Access. This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.