Transcriptome Analysis of Sorbic Acid-Stressed
            <i>Bacillus subtilis</i>
            Reveals a Nutrient Limitation Response and Indicates Plasma Membrane Remodeling

Beek, Alex Ter; Keijser, Bart J. F.; Boorsma, André; Zakrzewska, Anna; Orij, Rick; Smits, Gertien J.; Brul, Stanley

doi:10.1128/jb.01516-07

Cited by 56 publications

(72 citation statements)

References 80 publications

(72 reference statements)

Supporting

Mentioning

Contrasting

Order By: Relevance

“…(YkhA) was correlated with increased membrane remodeling (55). Therefore, thioesterases may play a critical role in the acylation/reacylation process of membrane remodeling.…”

Section: Discussionmentioning

confidence: 96%

Acyl Coenzyme A Thioesterase 7 Regulates Neuronal Fatty Acid Metabolism To Prevent Neurotoxicity

Ellis

Wong

Wolfgang

2013

Molecular and Cellular Biology

View full text Add to dashboard Cite

Numerous neurological diseases are associated with dysregulated lipid metabolism; however, the basic metabolic control of fatty acid metabolism in neurons remains enigmatic. Here we have shown that neurons have abundant expression and activity of the long-chain cytoplasmic acyl coenzyme A (acyl-CoA) thioesterase 7 (ACOT7) to regulate lipid retention and metabolism. Unbiased and targeted metabolomic analysis of fasted mice with a conditional knockout of ACOT7 in the nervous system, Acot7 N؊/؊ , revealed increased fatty acid flux into multiple long-chain acyl-CoA-dependent pathways. The alterations in brain fatty acid metabolism were concomitant with a loss of lean mass, hypermetabolism, hepatic steatosis, dyslipidemia, and behavioral hyperexcitability in Acot7 N؊/؊ mice. These failures in adaptive energy metabolism are common in neurodegenerative diseases. In agreement, Acot7 N؊/؊ mice exhibit neurological dysfunction and neurodegeneration. These data show that ACOT7 counterregulates fatty acid metabolism in neurons and protects against neurotoxicity. Neurons have a unique lipid composition that is critical for the development and function of the nervous system, and defects in lipid metabolism result in severe and debilitating neurological disease; however, there is a dearth of understanding about how neurons uniquely regulate intracellular fatty acid (FA) metabolism. There are numerous inborn errors of lipid metabolism that have clear neuropathological outcomes. Apart from these inborn errors of metabolism, it is becoming increasingly evident that many neurodegenerative diseases, including Alzheimer's disease, Parkinson's disease, and amyotrophic lateral sclerosis (ALS), have underlying metabolic dysfunction that often involves dysregulated lipid metabolism (1-5). A better understanding of neuronal metabolism is required to provide insight into neurological function and pathology, since dysregulated neurometabolism may contribute to the progression of diabetes and obesity and hasten neurodegeneration (6-8).Fatty acid metabolism in the nervous system has been shown to directly and profoundly regulate multiple aspects of animal physiology and behavior (9-14). Furthermore, ion channels that play a role in neuronal activation have been shown to be regulated by lipids either directly or indirectly (15)(16)(17)(18)(19)(20). Fatty acids are precursors for membrane biosynthesis, signaling lipids, posttranslational modification (e.g., palmitoylation), energy storage, and energy production. Although most neurons are not thought to rely on fatty acids to meet their cellular bioenergetic requirements, the brain has a unique fatty acid composition and metabolism that are critical for neural function. Due in part to the incredible heterogeneity of neurons themselves and the diversity of neuronal cell types in general, the means by which any neuronal population obtains or utilizes fatty acids is poorly understood.Fatty acids either made de novo or taken up from the diet require ligation to coenzyme A (CoA) for their cellular r...

show abstract

“…(YkhA) was correlated with increased membrane remodeling (55). Therefore, thioesterases may play a critical role in the acylation/reacylation process of membrane remodeling.…”

Section: Discussionmentioning

confidence: 96%

Acyl Coenzyme A Thioesterase 7 Regulates Neuronal Fatty Acid Metabolism To Prevent Neurotoxicity

Ellis

Wong

Wolfgang

2013

Molecular and Cellular Biology

View full text Add to dashboard Cite

show abstract

“…After 4 h of incubation at room temperature, absorbance at 520 nm was measured (using a NanoDrop spectrophotometer) and compared to a standard curve in CTRL medium (using 10 mM to 0.31 mM acetoin in 2-fold serial dilutions), which was linear for A 520 versus [acetoin] 0. 5 . The calculated acetoin produced in each treatment was normalized to the optical density (OD 600 ) of the cultures after 5.5 h of incubation, and the results were analyzed (in JMP) by oxygen condition with the ANOVA model [acetoin] ϭ diacetate ϫ lactate ϫ acetoin ϫ strain ϩ date ϩ E, where the fixed effects diacetate, lactate, acetoin, and strain represent the effects of the three metabolites in the treatment medium and the strains tested and these are fully crossed to estimate all possible interactions.…”

Section: ϫ7mentioning

confidence: 99%

“…To date, acid stress response studies of bacteria have focused on acid-adapted exponential-phase (7,34) or stationary-phase (41) cells or on transcription differences during acid shock (exposures of less than 1 h) (3,5). As the end goal of bacteriostatic growth-inhibiting treatments in foods is to indefinitely extend the lag phase, our work focused specifically on the transcriptomic response to organic acid stress under conditions approximating adaptation (8 h into lag phase) during refrigerated storage (7°C, microaerophilic conditions) of a food product (pH 6.1, 4.65% water-phase [w.p.]…”

mentioning

confidence: 99%

The Transcriptional Response of Listeria monocytogenes during Adaptation to Growth on Lactate and Diacetate Includes Synergistic Changes That Increase Fermentative Acetoin Production

Stasiewicz

Wiedmann

Bergholz

2011

Appl Environ Microbiol

View full text Add to dashboard Cite

The organic acids lactate and diacetate are commonly used in combination in ready-to-eat foods because they show synergistic ability to inhibit the growth of Listeria monocytogenes. Full-genome microarrays were used to investigate the synergistic transcriptomic responses of two L. monocytogenes strains, H7858 (serotype 4b) and F6854 (serotype 1/2a), to these two organic acids under conditions representing osmotic and cold stress encountered in foods. Strains were exposed to brain heart infusion (BHI) broth at 7°C with 4.65% water-phase (w.p.) NaCl at pH 6.1 with (i) 2% w.p. potassium lactate, (ii) 0.14% w.p. sodium diacetate, (iii) the combination of both at the same levels, or (iv) no organic acids as a control. RNA was extracted 8 h after exposure, during lag phase, to capture gene transcription changes during adaptation to the organic acid stress. Significant differential transcription of 1,041 genes in H7858 and 640 genes in F6854 was observed in at least one pair of the 4 different treatments. The effects of combined treatment with lactate and diacetate included (i) synergistic transcription differences for 474 and 209 genes in H7858 and F6854, respectively, (ii) differential transcription of genes encoding cation transporters and ABC transporters of metals, and (iii) altered metabolism, including induction of a nutrient-limiting stress response, reduction of menaquinone biosynthesis, and a shift from fermentative production of acetate and lactate to energetically less favorable, neutral acetoin. These data suggest that additional treatments that interfere with cellular energy generation processes could more efficiently inhibit the growth of L. monocytogenes.Listeria monocytogenes is a psychrotolerant food-borne pathogen that is of particular concern to the ready-to-eat-meat and -seafood industries because its ability to grow at temperatures as low as Ϫ0.4°C (70) reduces the ability of refrigeration to control the pathogen's growth in foods. Because L. monocytogenes generally contaminates foods at low levels (27) and has a high infectious dose (69), the ability of the organism to grow in foods is critical for its ability to cause disease (16). Foods do not support growth if they are stored frozen, have a pH of Յ4.4, have a water activity of Ͻ0.92, or incorporate some type of growth inhibiting measure (21), e.g., chemical preservatives (32). Ready-to-eat meat and seafood products have been identified as high-risk foods for listeriosis, as these foods support growth of L. monocytogenes (22), but it has also been predicted that reformulation of U.S. deli meats with effective growth inhibitors, e.g., the organic acids lactate and diacetate, would result in a 2-to 8-fold reduction of listeriosis due to consumption of these products (55). One particular advantage to using the combination of lactate and diacetate for L. monocytogenes control in meat and seafood products is that these inhibitors have been shown to have greater-than-additive, i.e., synergistic, growth-inhibiting effects (65), although the mechanisms...

show abstract

“…To investigate this activation at the transcriptome level, we compared light and dark samples, taken during typical experiments for the two light responses, with microarray analyses (see Materials and Methods). The results were analyzed using T-profiler, a tool that identifies significantly regulated gene groups, using all data derived from the microarray experiments (7,51). Table 3 shows the gene groups that were significantly upregulated in response to visible light in both experiments.…”

Section: B Activation Is Enhanced By Light In Stationary Phase In Amentioning

confidence: 99%

“…Data were analyzed in two independent ways. First, the 2-log ratios of all genes in the data set were analyzed using T-profiler (7), adapted for B. subtilis (51). This tool uses t tests to determine the significance of the total changes in predefined groups of genes.…”

mentioning

confidence: 99%

Red Light Activates the σ^B-Mediated General Stress Response ofBacillus subtilisvia the Energy Branch of the Upstream Signaling Cascade

et al. 2010

View full text Add to dashboard Cite

When the common soil bacterium Bacillus subtilis is starved or exposed to any of a range of stresses, a complex signal transduction network is activated. This then leads to activation of the alternative RNA polymerase subunit B , which controls a stress response regulon composed of more than 150 genes (19,44,55), of which the ctc gene has generally been accepted as the prototype representative (19). The genes from this B regulon encode proteins from several different functional categories, including transcriptional regulation, cell protection (like carotenoid biosynthesis and the expression of catalase activity), influx and efflux processes, and carbon metabolism (20). The B response can be activated by two separate, but converging, branches of a very complex signal transduction network. These two branches are responsive to different stress signals, as follows: the energy stress branch (elicited by carbon, oxygen, or phosphate limitation) leads to the activation of RsbP, whereas the environmental stress branch (elicited by addition of, e.g., salt or ethanol) activates RsbU. Both RsbP and RsbU are specific phosphatases of the phosphorylated form of RsbV (phosphorylated on a serine residue), which indirectly leads to activation of B (for reviews, see references 19, 32, and 55). Signaling through the environmental branch involves a large, complex structure, called the stressosome (14, 31), for sensory input. This structure is larger than 1.5 MDa and contains the RsbS, RsbT, and RsbRA proteins and several paralogues of RsbRA (14,26). Activation of the stressosome leads to RsbT release, which in turn activates RsbU (15).It has been reported that the B response in B. subtilis can be activated with blue light via involvement of the phototropin homologue YtvA (4,17,49). This protein contains a single LOV (light oxygen voltage) domain (21) that binds a flavin cofactor and shows an authentic photocycle with a very slow thermal recovery rate of its stable ground state (28). It functions in the environmental stress branch of the upstream signal transduction network that regulates activation of B . It is one of the paralogues of RsbRA, but so far, no evidence has been provided to show that YtvA forms an (integral) part of the stressosome. In this study we show that B can also be activated with light through the energy stress branch of this cascade, via the RsbP protein. This second light response is preferentially activated by red light. Significantly, transcriptome analyses confirm that YtvA-dependent and -independent light effects upregulate the B regulon. MATERIALS AND METHODSBacterial strains and genetic manipulation. The bacterial strains, plasmids, and primers used in this investigation are listed in Table 1. DNA manipulations and molecular genetic techniques were carried out using standard procedures. The strains PB565 (2), PB567 (57), and PB605 (11) were provided by C. Price (University of California at Davis) and were constructed using previously published procedures (Table 1). Escherichia coli MC1061 was used as th...

show abstract

Transcriptome Analysis of Sorbic Acid-Stressed Bacillus subtilis Reveals a Nutrient Limitation Response and Indicates Plasma Membrane Remodeling

Cited by 56 publications

References 80 publications

Acyl Coenzyme A Thioesterase 7 Regulates Neuronal Fatty Acid Metabolism To Prevent Neurotoxicity

Acyl Coenzyme A Thioesterase 7 Regulates Neuronal Fatty Acid Metabolism To Prevent Neurotoxicity

The Transcriptional Response of Listeria monocytogenes during Adaptation to Growth on Lactate and Diacetate Includes Synergistic Changes That Increase Fermentative Acetoin Production

Red Light Activates the σ^B-Mediated General Stress Response ofBacillus subtilisvia the Energy Branch of the Upstream Signaling Cascade

Contact Info

Product

Resources

About

Transcriptome Analysis of Sorbic Acid-Stressed Bacillus subtilis Reveals a Nutrient Limitation Response and Indicates Plasma Membrane Remodeling

Cited by 56 publications

References 80 publications

Acyl Coenzyme A Thioesterase 7 Regulates Neuronal Fatty Acid Metabolism To Prevent Neurotoxicity

Acyl Coenzyme A Thioesterase 7 Regulates Neuronal Fatty Acid Metabolism To Prevent Neurotoxicity

The Transcriptional Response of Listeria monocytogenes during Adaptation to Growth on Lactate and Diacetate Includes Synergistic Changes That Increase Fermentative Acetoin Production

Red Light Activates the σB-Mediated General Stress Response ofBacillus subtilisvia the Energy Branch of the Upstream Signaling Cascade

Contact Info

Product

Resources

About

Red Light Activates the σ^B-Mediated General Stress Response ofBacillus subtilisvia the Energy Branch of the Upstream Signaling Cascade