The growth‐survival trade‐off is hard‐wired in the <i>Lactococcus lactis</i> gene regulation network

Ercan, Onur; Besten, H.M.W. den; Smid, Eddy J.; Kleerebezem, Michiel

doi:10.1111/1758-2229.13073

Cited by 6 publications

(11 citation statements)

References 32 publications

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“…These results indicate that retentostat grown B. breve NRBB57 cells can activate a multiple stress defence, with a prominent relative increase in oxidative stress survival capacity. Comparing B. breve stress survival capacity with that of Lactococcus lactis and Lactiplantibacillus plantarum retentostat cells exposed to similar stresses, shows higher stress tolerance of the latter species (Ercan et al, 2022). It should be noted that in the current experimental set up, no additional measures were taken to prevent exposure to oxygen in the stress survival experiments.…”

Section: Stress Tolerance To High Temperatures Low Ph and Oxidative S...mentioning

confidence: 81%

“…Recent studies describe the use of the so-called retentostat cultivation to determine the impact of near-zero growth rates on microbial physiology including activation of stress resistance (Ercan et al, 2022;Goffin et al, 2010;Vos et al, 2016). Retentostat cultivation is a variation on the classical chemostat cultivation and ensures complete retention of cells by inserting a cross-flow filter in the effluent line.…”

Section: Introductionmentioning

confidence: 99%

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Enhanced stress resistance of Bifidobacterium breve NRBB57 by induction of stress proteins at near-zero growth rates

Camargo

Mastrigt

Bongers

et al. 2023

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Bifidobacterium breve is a common habitant of the human gut and is used as probiotic in functional foods. B. breve has to cope with multiple stress conditions encountered during processing and passage through the human gut, including high temperature, low pH and exposure to oxygen. Additionally, during industrial processing and in the gut, B. breve could encounter nutrient limitation resulting in reduced growth rates that can trigger adaptive stress responses. For this reason, it is important to develop culture methods that elicit resistance to multiple stresses (robustness) encountered by the bacteria. To investigate the impact of caloric restriction on robustness of the probiotic B. breve NRBB57, this strain was grown in lactose-limited chemostat cultures and in retentostat for 21 days, at growth rates ranging from 0.4 h-1 to 0.00081 h-1. Proteomes of cells harvested at different growth rates were correlated to acid, hydrogen peroxide and heat stress survival capacity. Comparative proteome analysis showed that retentostat-grown cells had significantly increased abundance of a variety of stress proteins involved in protein quality maintenance and DNA repair (DnaJ, Hsp90, FtsH, ClpB, ClpP1, ClpC, GroES, RuvB, RecA), as well as proteins involved in oxidative stress defence (peroxiredoxin, ferredoxin, thioredoxin peroxidase, glutaredoxin and thioredoxin reductase). Exposure to three different stress conditions, 45 °C, pH 3, and 10 mM H2O2, showed highest stress resistance of retentostat cells sampled at week 2 and week 3 grown at 0.0018 and 0.00081 h-1. Our findings show that cultivation at near-zero growth rates induces higher abundance of stress defence proteins contributing to the robustness of B. breve NRBB57, thereby offering an approach that may support its production and functionality.

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Section: Stress Tolerance To High Temperatures Low Ph and Oxidative S...mentioning

confidence: 81%

Section: Introductionmentioning

confidence: 99%

Enhanced stress resistance of Bifidobacterium breve NRBB57 by induction of stress proteins at near-zero growth rates

Camargo

Mastrigt

Bongers

et al. 2023

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“…Catabolic flexibility, a bacterial physiological status under which a wider range of substrates can be utilized [ 46 ], is often induced in cells with a reduced growth rate [ 45 ]. Furthermore, growth rate reduction has been shown in different bacterial species to govern their resistance to different stresses [ 26 , 27 , 28 , 58 , 59 ]. A few studies using bifidobacteria have evidenced some of these features.…”

Section: Conclusion and Discussionmentioning

confidence: 99%

The Pleiotropic Effects of Carbohydrate-Mediated Growth Rate Modifications in Bifidobacterium longum NCC 2705

et al. 2023

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Bifidobacteria are saccharolytic bacteria that are able to metabolize a relatively large range of carbohydrates through their unique central carbon metabolism known as the “bifid-shunt”. Carbohydrates have been shown to modulate the growth rate of bifidobacteria, but unlike for other genera (e.g., E. coli or L. lactis), the impact it may have on the overall physiology of the bacteria has not been studied in detail to date. Using glucose and galactose as model substrates in Bifidobacterium longum NCC 2705, we established that the strain displayed fast and slow growth rates on those carbohydrates, respectively. We show that these differential growth conditions are accompanied by global transcriptional changes and adjustments of central carbon fluxes. In addition, when grown on galactose, NCC 2705 cells were significantly smaller, exhibited an expanded capacity to import and metabolized different sugars and displayed an increased acid-stress resistance, a phenotypic signature associated with generalized fitness. We predict that part of the observed adaptation is regulated by the previously described bifidobacterial global transcriptional regulator AraQ, which we propose to reflect a catabolite-repression-like response in B. longum. With this manuscript, we demonstrate that not only growth rate but also various physiological characteristics of B. longum NCC 2705 are responsive to the carbon source used for growth, which is relevant in the context of its lifestyle in the human infant gut where galactose-containing oligosaccharides are prominent.

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“…In the retentostat, a constant volume of fresh medium is input into the culture vessel, but the whole culture is not simultaneously discarded. Instead, the culture is filtered, the cells are returned to the culture vessel, and only the used medium is discarded [ 87 , 88 , 89 , 90 ]. This strategy leads to a progressive accumulation of cells in the culture vessel so that a higher number of cells need to share the same amount of nutrients.…”

Section: Microbial Growthmentioning

confidence: 99%

“…When nutrients are scarce or conditions are growth-restrictive, a number of microorganisms (many are still to be tested) can thrive by drastically reducing their growth to near-zero rates. Microorganisms cultured at a near-zero growth rate are viable and active cells [ 87 , 88 , 89 , 90 , 104 , 107 ] but the environmental limitations restrict their growth to a very slow rate. These cells at a near-zero growth rate are at a very different state than cells undergoing survival or decline (death) or at the stationary phase, as these latter processes occur when cells are no longer growing, they might show poor or null activity, and they (or a large fraction of the cells) are likely to be non-viable and/or non-culturable [ 108 ].…”

Section: Growth At Near-zero Rate (Severe Growth Limitation)mentioning

confidence: 99%

Microbial Growth under Limiting Conditions-Future Perspectives

Gonzalez

Aranda

2023

Microorganisms

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Microorganisms rule the functioning of our planet and each one of the individual macroscopic living creature. Nevertheless, microbial activity and growth status have always been challenging tasks to determine both in situ and in vivo. Microbial activity is generally related to growth, and the growth rate is a result of the availability of nutrients under adequate or adverse conditions faced by microbial cells in a changing environment. Most studies on microorganisms have been carried out under optimum or near-optimum growth conditions, but scarce information is available about microorganisms at slow-growing states (i.e., near-zero growth and maintenance metabolism). This study aims to better understand microorganisms under growth-limiting conditions. This is expected to provide new perspectives on the functions and relevance of the microbial world. This is because (i) microorganisms in nature frequently face conditions of severe growth limitation, (ii) microorganisms activate singular pathways (mostly genes remaining to be functionally annotated), resulting in a broad range of secondary metabolites, and (iii) the response of microorganisms to slow-growth conditions remains to be understood, including persistence strategies, gene expression, and cell differentiation both within clonal populations and due to the complexity of the environment.

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The growth‐survival trade‐off is hard‐wired in the Lactococcus lactis gene regulation network

Cited by 6 publications

References 32 publications

Enhanced stress resistance of Bifidobacterium breve NRBB57 by induction of stress proteins at near-zero growth rates

Enhanced stress resistance of Bifidobacterium breve NRBB57 by induction of stress proteins at near-zero growth rates

The Pleiotropic Effects of Carbohydrate-Mediated Growth Rate Modifications in Bifidobacterium longum NCC 2705

Microbial Growth under Limiting Conditions-Future Perspectives

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