Stationary Lactococcus cremoris: Energetic State, Protein Synthesis Without Nitrogen and Their Effect on Survival

Sieze Douwenga, Rinke J. van Tatenhove-Pel, Emile Zwering, Herwig Bachmann*

*Corresponding author for this work

Research output: Contribution to JournalArticleAcademicpeer-review


During storage and ripening of fermented foods, Lactococcus cremoris is predominantly in a non-growing state. L. cremoris can become stationary due to starvation or acidification, and its metabolism in these non-growing states affects the fermented product. Available studies on the response of L. cremoris to acid and starvation stress are based on population level data. We here characterized the energetic state and the protein synthesis capacity of stationary L. cremoris cultures at the single cell level. We show that glucose starved stationary cells are energy-depleted, while acid-induced stationary cells are energized and can maintain a pH gradient over their membrane. In the absence of glucose and arginine, a small pH gradient can still be maintained. Subpopulations of stationary cells can synthesize protein without a nitrogen source, and the subpopulation size decreases with increasing stationary phase length. Protein synthesis capacity during starvation only benefits culturability after 6 days. These results highlight significant differences between glucose starved stationary and acid-induced stationary cells. Furthermore, they show that the physiology of stationary phase L. cremoris cells is multi-facetted and heterogeneous, and the presence of an energy source during stationary phase impacts the cells capacity to adapt to their environment.

Original languageEnglish
Article number794316
Pages (from-to)1-10
Number of pages10
JournalFrontiers in Microbiology
Issue numberDecember
Early online date17 Dec 2021
Publication statusPublished - Dec 2021

Bibliographical note

Funding Information:
RTP was partly financed by Netherlands Organisation for Scientific Research (NWO), as part of the research programme TTW with project number 13858. SD and HB were funded by TiFN program 16MF01, Wageningen, Netherlands.

Funding Information:
Wegmann, U., O’Connell-Motherway, M., Zomer, A., Buist, G., Shearman, C., Canchaya, C., et al. (2007). Complete genome sequence of the prototype lactic acid bacterium Lactococcus lactis subsp. cremoris MG1363. J. Bacteriol. 189, 3256–3270. doi: 10.1128/JB.01768-06 Wels, M., Siezen, R., van Hijum, S., Kelly, W. J., and Bachmann, H. (2019). Comparative genome analysis of Lactococcus lactis indicates niche adaptation and resolves genotype/phenotype disparity. Front. Microbiol. 10:4. doi: 10.3389/ fmicb.2019.00004 Zhang, H., Lyu, Z., Fan, Y., Evans, C. R., Barber, K. W., Banerjee, K., et al. (2020). Metabolic stress promotes stop-codon readthrough and phenotypic heterogeneity. Proc. Natl. Acad. Sci. U.S.A. 117, 22167–22172. doi: 10.1073/ pnas.2013543117 Conflict of Interest: This project was partially organized by and executed under the auspices of TiFN, a public-private partnership on precompetitive research in food and nutrition. Funding for this research was obtained from FrieslandCampina (Wageningen, Netherlands), CSK Food Enrichment (Wageningen, Netherlands), and the Top-sector Agri&Food. HB is employed by NIZO a contract research organization.

Publisher Copyright:
Copyright © 2021 Douwenga, van Tatenhove-Pel, Zwering and Bachmann.


  • energetic state
  • protein synthesis
  • proton gradient
  • single cell
  • starvation
  • stationary phase
  • survival


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