Characterization of the individual glucose uptake systems of <i>Lactococcus lactis</i>: mannose‐PTS, cellobiose‐PTS and the novel GlcU permease

Castro, Rute; Neves, Ana Rute; Fonseca, Luis L.; Pool, Wietske A.; Kok, Jan; Kuipers, Oscar P.; Santos, Helena

doi:10.1111/j.1365-2958.2008.06564.x

Cited by 75 publications

(89 citation statements)

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“…The maximal concentration of the glycolytic intermediate FBP was elevated in the ldh mutant compared to the wild type. A similar pattern has been reported for an LDH-deficient strain of Lactococcus lactis (11), an organism for which an inverse relationship between FBP accumulation and glucose consumption was established (30). This association holds true for S. pneumoniae (Fig.…”

Section: Discussionsupporting

confidence: 57%

Lactate Dehydrogenase Is the Key Enzyme for Pneumococcal Pyruvate Metabolism and Pneumococcal Survival in Blood

et al. 2014

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Streptococcus pneumoniae is a fermentative microorganism and causes serious diseases in humans, including otitis media, bacteremia, meningitis, and pneumonia. However, the mechanisms enabling pneumococcal survival in the host and causing disease in different tissues are incompletely understood. The available evidence indicates a strong link between the central metabolism and pneumococcal virulence. To further our knowledge on pneumococcal virulence, we investigated the role of lactate dehydrogenase (LDH), which converts pyruvate to lactate and is an essential enzyme for redox balance, in the pneumococcal central metabolism and virulence using an isogenic ldh mutant. Loss of LDH led to a dramatic reduction of the growth rate, pinpointing the key role of this enzyme in fermentative metabolism. The pattern of end products was altered, and lactate production was totally blocked. The fermentation profile was confirmed by in vivo nuclear magnetic resonance (NMR) measurements of glucose metabolism in nongrowing cell suspensions of the ldh mutant. In this strain, a bottleneck in the fermentative steps is evident from the accumulation of pyruvate, revealing LDH as the most efficient enzyme in pyruvate conversion. An increase in ethanol production was also observed, indicating that in the absence of LDH the redox balance is maintained through alcohol dehydrogenase activity. We also found that the absence of LDH renders the pneumococci avirulent after intravenous infection and leads to a significant reduction in virulence in a model of pneumonia that develops after intranasal infection, likely due to a decrease in energy generation and virulence gene expression.

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Section: Discussionsupporting

confidence: 57%

Lactate Dehydrogenase Is the Key Enzyme for Pneumococcal Pyruvate Metabolism and Pneumococcal Survival in Blood

et al. 2014

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“…These nucleotide substitutions affect the following genes: gltX, aroD, pepF, ptcC, and groEL, all encoding basal functions of the cell. ptcC encodes the IIC component of the cellobiose-specific phosphotransferase system (PTS), involved in glucose and cellobiose transport and metabolism (5,13). The chaperonin GroEL is an HSP60 family protein involved in the productive folding of proteins under stressful conditions (e.g., elevated temperatures) (6).…”

Section: Resultsmentioning

confidence: 99%

Genome Sequences of Lactococcus lactis MG1363 (Revised) and NZ9000 and Comparative Physiological Studies

2010

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Lactococcus lactis NZ9000 and its parent MG1363 are the most commonly used lactic acid bacteria for expression and physiological studies. We noted unexpected but significant differences in the growth behaviors of both strains. We sequenced the entire genomes of the original NZ9000 and MG1363 strains using an ultradeep sequencing strategy. The analysis of the L. lactis NZ9000 genome yielded 79 differences, mostly point mutations, with the annotated genome sequence of L. lactis MG1363. Resequencing of the MG1363 strain revealed that 73 out of the 79 differences were due to errors in the published sequence. Comparative transcriptomic studies revealed several differences in the regulation of genes involved in sugar fermentation, which can be explained by two specific mutations in a region of the ptcC promoter with a key role in the regulation of cellobiose and glucose uptake.

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“…S6), which encodes a component of the main glucose transport system of L. lactis. This phosphoenolpyruvate: phosphotransferase system (designated PTS Man because of its initial description as a mannose transporter) is the only high-affinity glucose transporter in this strain (K m = 13 μM), whereas the other glucose transport systems, the glucose permease glcU and the PTS Cel system (a PTS that is also known to transport cellobiose) have K m values of 2.4 mM and 8.7 mM, respectively (18). The sugar concentration at the beginning of our batch cultures was 5 mM and therefore mutations in the high-affinity system are expected to have the largest effects on glucose transport in our selection medium.…”

Section: Major Metabolic Shift Caused Decreased Growth Rate But Incrementioning

confidence: 99%

Availability of public goods shapes the evolution of competing metabolic strategies

Bachmann¹,

Fischlechner

Rabbers³

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

173

220

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Tradeoffs provide a rationale for the outcome of natural selection. A prominent example is the negative correlation between the growth rate and the biomass yield in unicellular organisms. This tradeoff leads to a dilemma, where the optimization of growth rate is advantageous for an individual, whereas the optimization of the biomass yield would be advantageous for a population. High-rate strategies are observed in a broad variety of organisms such as Escherichia coli, yeast, and cancer cells. Growth in suspension cultures favors fast-growing organisms, whereas spatial structure is of importance for the evolution of high-yield strategies. Despite this realization, experimental methods to directly select for increased yield are lacking. We here show that the serial propagation of a microbial population in a water-in-oil emulsion allows selection of strains with increased biomass yield. The propagation in emulsion creates a spatially structured environment where the growth-limiting substrate is privatized for populations founded by individual cells. Experimental evolution of several isogenic Lactococcus lactis strains demonstrated the existence of a tradeoff between growth rate and biomass yield as an apparent Pareto front. The underlying mutations altered glucose transport and led to major shifts between homofermentative and heterofermentative metabolism, accounting for the changes in metabolic efficiency. The results demonstrated the impact of privatizing a public good on the evolutionary outcome between competing metabolic strategies. The presented approach allows the investigation of fundamental questions in biology such as the evolution of cooperation, cell-cell interactions, and the relationships between environmental and metabolic constraints.A lthough the existence of tradeoffs in evolution seems to be undisputable, experimental evidence obtained under controlled conditions is scarce. Several examples failed to show tradeoffs (1-4), whereas others could find them (5, 6) or found general but not universal tradeoffs (7,8). A tradeoff between growth rate and growth yield in microbes (9-11) has direct implications for experiments carried out in liquid cultures. This is especially of importance during prolonged cultivations such as laboratory evolution experiments. In suspension, fast-growing variants outcompete slower growing ones at the cost of biomass yield (5). The yield versus rate optimization is governed by a dilemma where fast growth is advantageous from the perspective of an individual cell, whereas slow growth, and therefore high yield, is advantageous from the perspective of a population. This dilemma is consistent with a concept termed the tragedy of the commons (12). It is well described that spatial structure is essential for the selection of high-yield strategies (13-15). The yield/rate tradeoff of microbial growth has been linked to metabolic strategies (11) such as the switch between respiration and fermentation in yeast (9). It is suggested that the underlying cause of this tradeoff is based on...

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Characterization of the individual glucose uptake systems of Lactococcus lactis: mannose‐PTS, cellobiose‐PTS and the novel GlcU permease

Cited by 75 publications

References 50 publications

Lactate Dehydrogenase Is the Key Enzyme for Pneumococcal Pyruvate Metabolism and Pneumococcal Survival in Blood

Lactate Dehydrogenase Is the Key Enzyme for Pneumococcal Pyruvate Metabolism and Pneumococcal Survival in Blood

Genome Sequences of Lactococcus lactis MG1363 (Revised) and NZ9000 and Comparative Physiological Studies

Availability of public goods shapes the evolution of competing metabolic strategies

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