Growth rate regulated genes and their wide involvement in the Lactococcus lactis stress responses

Dressaire, Clémentine; Redon, Emma; Milhem, Hélène; Besse, Philippe; Loubière, Pascal; Cocaign‐Bousquet, Muriel

doi:10.1186/1471-2164-9-343

Cited by 47 publications

(65 citation statements)

References 35 publications

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“…It is intriguing to speculate that the intrachromosomal heterogeneity of the periodic signal and associated DNA curvature could play a role in regulation of gene expression. It has been known that chromosomal location of genes in prokaryotes is not random, but the nonrandomness has been generally ascribed to locations relative to the origin and terminus of replication, colocalization of coexpressed genes, or evolutionary constraints related to lateral gene transfer or gene amplification (6,8,15,25,31,32). We propose that heterogeneity of physical structure of the nucleoid reflected in the intrachromosomal variance of sequence periodicity can serve as an additional constraint on gene location, possibly by modulating the gene expression in different chromosomal regions.…”

Section: Discussionmentioning

confidence: 99%

Comparative Analysis of Sequence Periodicity among Prokaryotic Genomes Points to Differences in Nucleoid Structure and a Relationship to Gene Expression

Mrázek

2010

J Bacteriol

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Regular spacing of short runs of A or T nucleotides in DNA sequences with a period close to the helical period of the DNA double helix has been associated with intrinsic DNA bending and nucleosome positioning in eukaryotes. Analogous periodic signals were also observed in prokaryotic genomes. While the exact role of this periodicity in prokaryotes is not known, it has been proposed to facilitate the DNA packaging in the prokaryotic nucleoid and/or to promote negative or positive supercoiling. We developed a methodology for assessments of intragenomic heterogeneity of these periodic patterns and applied it in analysis of 1,025 prokaryotic chromosomes. This technique allows more detailed analysis of sequence periodicity than previous methods where sequence periodicity was assessed in an integral form across the whole chromosome. We found that most genomes have the periodic signal confined to several chromosomal segments while most of the chromosome lacks a strong sequence periodicity. Moreover, there are significant differences among different prokaryotes in both the intensity and persistency of sequence periodicity related to DNA curvature. We proffer that the prokaryotic nucleoid consists of relatively rigid sections stabilized by short intrinsically bent DNA segments and characterized by locally strong periodic patterns alternating with regions featuring a weak periodic signal, which presumably permits higher structural flexibility. This model applies to most bacteria and archaea. In genomes with an exceptionally persistent periodic signal, highly expressed genes tend to concentrate in aperiodic sections, suggesting that structural heterogeneity of the nucleoid is related to local differences in transcriptional activity.DNA sequences generally contain two strong periodic signals. The dominant signal has a period of 3 bp and relates to biased codon and amino acid usages in protein-coding genes. The second significant periodic signal has a period close to 10.5 bp (the average length of a helical turn of DNA in the canonical B conformation) and relates to DNA curvature and/or bendability. This periodic signal is most pronounced in the distribution of short runs of A or T (37,39,40). In eukaryotes, the DNA periodicity is a primary nucleosome positioning signal-the intrinsically bent DNA both facilitates wrapping of the DNA around the histone core and restricts the placement of nucleosomes (22,35,36,40). The periodic pattern in the DNA sequence can influence characteristics of the chromatin and consequently the molecular interactions associated with transcription. In particular, patterns of sequence periodicity in the Caenorhabditis elegans genome are related to histone modifications, and regions with strong periodic signals are associated with germ line-specific genes, suggesting that periodicity within chromosomal segments can affect levels of gene expression (9,12,17).Previous analyses of periodic signals in prokaryotic DNA sequences raised interesting questions about possible roles the sequence periodicity and c...

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Section: Discussionmentioning

confidence: 99%

Comparative Analysis of Sequence Periodicity among Prokaryotic Genomes Points to Differences in Nucleoid Structure and a Relationship to Gene Expression

Mrázek

2010

J Bacteriol

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“…The results indicated that in C. crescentus spoT is required for expression of cspD, either via a direct effect of ppGpp on its transcription or indirectly by the effects on the overall cell response to carbon starvation and growth. In a global analysis of Lactobacillus lactis gene expression in response to carbon limitation (isoleucine or glucose starvation), the stringent response and growth rate were compared, and the results showed that the stringent response is not the general mechanism controlling growth rate modifications or glucose starvation (11).…”

Section: Discussionmentioning

confidence: 99%

SpdR, a Response Regulator Required for Stationary-Phase Induction of Caulobacter crescentus cspD

et al. 2010

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The cold shock protein (CSP) family includes small polypeptides that are induced upon temperature downshift and stationary phase. The genome of the alphaproteobacterium Caulobacter crescentus encodes four CSPs, with two being induced by cold shock and two at the onset of stationary phase. In order to identify the environmental signals and cell factors that are involved in cspD expression at stationary phase, we have analyzed cspD transcription during growth under several nutrient conditions. The results showed that expression of cspD was affected by the medium composition and was inversely proportional to the growth rate. The maximum levels of expression were decreased in a spoT mutant, indicating that ppGpp may be involved in the signalization for carbon starvation induction of cspD. A Tn5 mutant library was screened for mutants with reduced cspD expression, and 10 clones that showed at least a 50% reduction in expression were identified. Among these, a strain with a transposon insertion into a response regulator of a two-component system showed no induction of cspD at stationary phase. This protein (SpdR) was able to acquire a phosphate group from its cognate histidine kinase, and gel mobility shift assay and DNase I footprinting experiments showed that it binds to an inverted repeat sequence of the cspD regulatory region. A mutated SpdR with a substitution of the conserved aspartyl residue that is the probable phosphorylation site is unable to bind to the cspD regulatory region and to complement the spdR mutant phenotype.

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“…Hybridization signals were quantified and statistically treated as previously described (10,34,35). Briefly, the local background was removed, and signals were normalized by the mean intensity of the corresponding membrane.…”

Section: Methodsmentioning

confidence: 99%

Dynamic Analysis of the Lactococcus lactis Transcriptome in Cheeses Made from Milk Concentrated by Ultrafiltration Reveals Multiple Strategies of Adaptation to Stresses

Cretenet

Laroute

Ulvé

et al. 2011

Appl Environ Microbiol

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Lactococcus lactis is used extensively for the production of various cheeses. At every stage of cheese fabrication, L. lactis has to face several stress-generating conditions that result from its own modification of the environment as well as externally imposed conditions. We present here the first in situ global gene expression profile of L. lactis in cheeses made from milk concentrated by ultrafiltration (UF-cheeses), a key economical cheese model. The transcriptomic response of L. lactis was analyzed directly in a cheese matrix, starting from as early as 2 h and continuing for 7 days. The growth of L. lactis stopped after 24 h, but metabolic activity was maintained for 7 days. Conservation of its viability relied on an efficient proteolytic activity measured by an increasing, quantified number of free amino acids in the absence of cell lysis. Extensive downregulation of genes under CodY repression was found at day 7. L. lactis developed multiple strategies of adaptation to stressful modifications of the cheese matrix. In particular, expression of genes involved in acidic-and oxidativestress responses was induced. L. lactis underwent unexpected carbon limitation characterized by an upregulation of genes involved in carbon starvation, principally due to the release of the CcpA control. We report for the first time that in spite of only moderately stressful conditions, lactococci phage is repressed under UF-cheese conditions. Lactic acid bacteria, particularly Lactococcus lactis, have a long history of use in milk fermentation, from small-scale traditional operations to well-controlled industrial applications. Recent developments of molecular tools have unraveled the genetics, physiology, and metabolism of this economically very important microorganism. However, interpretation has always been limited by the lack of knowledge regarding in situ bacterial physiology. Technological properties (e.g., acidification, proteolytic or lipolytic activity, and bacteriocin production) can easily be shown and quantified in vitro but have hardly ever been verified in a complex solid matrix, due to local intrinsic factors. There have been several successful attempts to measure the DNA and rRNA extracted directly from a solid food (or environmental) matrix in order to estimate either the predominant species and/or the overall level of metabolic activity of the species (11,33). In a few cases, the expression of genes of technological interest from extracted mRNAs has been checked (42). The global gene or protein expression of L. lactis has been characterized in milk (15, 34) but not directly in cheese, the corresponding solid dairy matrix.Over the last few years, functional-genomics approaches, including transcriptomics, have been increasingly used to obtain global gene expression profiles, thereby providing a comprehensive view of microorganism physiology. So far, such global approaches in food microbiology and in situ have been poorly documented. Recently, Bachmann et al. presented the genetic responses of L. lactis in mixed cu...

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Growth rate regulated genes and their wide involvement in the Lactococcus lactis stress responses

Cited by 47 publications

References 35 publications

Comparative Analysis of Sequence Periodicity among Prokaryotic Genomes Points to Differences in Nucleoid Structure and a Relationship to Gene Expression

Comparative Analysis of Sequence Periodicity among Prokaryotic Genomes Points to Differences in Nucleoid Structure and a Relationship to Gene Expression

SpdR, a Response Regulator Required for Stationary-Phase Induction of Caulobacter crescentus cspD

Dynamic Analysis of the Lactococcus lactis Transcriptome in Cheeses Made from Milk Concentrated by Ultrafiltration Reveals Multiple Strategies of Adaptation to Stresses

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