Poly-β-hydroxybutyrate Metabolism Is Unrelated to the Sporulation and Parasporal Crystal Protein Formation in Bacillus thuringiensis

Wang, Xun; Zhou, Li; Li, Xin; Qian, Hongliang; Cai, Xia; Li, Xinfeng; He, Jin

doi:10.3389/fmicb.2016.00836

Cited by 17 publications

(22 citation statements)

References 48 publications

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“…1B). Considering the influence of different nutritional conditions and the controversy in the literature concerning the impact of PHB biosynthesis pathway on the growth characteristics of Bacillus and other bacterial species (Chen et al, 2012;Wang et al, 2016;Cevallos et al, 1996;Korotkova and Lidstrom, 2001) we examined the growth of the B. anthracis phaBC mutant in sporulation (DSM) and glucose-containing (TSB) media. The results of these experiments demonstrated that inactivation of the PHB biosynthesis pathway in B. anthracis does not lead to a notable difference in growth compared to the wild-type strain in both media (Fig.…”

Section: Resultsmentioning

confidence: 99%

“…For example, Chen et al . () found that the loss of PHB production in B. thuringiensis resulted in a growth delay and sporulation‐deficient phenotype, whereas another group reported that PHB metabolism does not affect growth and sporulation in this species (Wang et al ., ).…”

Section: Introductionmentioning

confidence: 99%

“…In spite of this, the role of the PHB accumulation and mobilization during sporulation for some species is still obscure. For example, Chen et al (2012) found that the loss of PHB production in B. thuringiensis resulted in a growth delay and sporulation-deficient phenotype, whereas another group reported that PHB metabolism does not affect growth and sporulation in this species (Wang et al, 2016).…”

Section: Introductionmentioning

confidence: 99%

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Poly(3‐hydroxybutyrate) fuels the tricarboxylic acid cycle and de novo lipid biosynthesis during Bacillus anthracis sporulation

Sadykov

Ahn

Widhelm

et al. 2017

Molecular Microbiology

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Numerous bacteria accumulate poly(3-hydroxybutyrate) (PHB) as an intracellular reservoir of carbon and energy in response to imbalanced nutritional conditions. In Bacillus spp., where PHB biosynthesis precedes the formation of the dormant cell type called the spore (sporulation), the direct link between PHB accumulation and efficiency of sporulation was observed in multiple studies. Although the idea of PHB as an intracellular carbon and energy source fueling sporulation was proposed several decades ago, the mechanisms underlying PHB contribution to sporulation have not been defined. Here, we demonstrate that PHB deficiency impairs Bacillus anthracis sporulation through diminishing the energy status of the cells and by reducing carbon flux into the tricarboxylic acid (TCA) cycle and de novo lipid biosynthesis. Consequently, this metabolic imbalance decreased biosynthesis of the critical components required for spore integrity and resistance, such as dipicolinic acid (DPA) and the spore's inner membrane. Supplementation of the PHB deficient mutant with exogenous fatty acids overcame these sporulation defects, highlighting the importance of the TCA cycle and lipid biosynthesis during sporulation. Combined, the results of this work reveal the molecular mechanisms of PHB contribution to B. anthracis sporulation and provide valuable insight into the metabolic requirements for this developmental process in Bacillus species.

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Section: Resultsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Poly(3‐hydroxybutyrate) fuels the tricarboxylic acid cycle and de novo lipid biosynthesis during Bacillus anthracis sporulation

Sadykov

Ahn

Widhelm

et al. 2017

Molecular Microbiology

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“…Taken together, these results indicate that the PHB synthesis and utilization processes occurred simultaneously in these cells. In another research using mutant B. thuringiensis BMB171 as a model organism, PHB degradation remained active even when the gene encoding for 3-oxoadipate enollactonase was deleted, which implies that other enzymes are responsible for PHB degradation as well [55]. The enzyme 3-oxoadipate enol-lactonase of B. thuringiensis contains a lipase box-like sequence (G-W-S102-M-G), and the serine (102) site was proved to be important for the PHB-hydrolyzing activity [22].…”

Section: Discussionmentioning

confidence: 99%

Proteome Profile Changes During Poly-hydroxybutyrate Intracellular Mobilization in Gram Positive Bacillus cereus tsu1

O’Hair

Thapa

et al. 2019

Preprint

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Background Bacillus cereus is a bacterium species can grow efficiently on a wide range of carbon sources and accumulate biopolymer poly-hydroxybutyrate (PHB) up to 80% cell dry weight. PHB is an aliphatic polymer produced and stored intracellularly as a reservoir of carbon and energy, its mobilization is a key biological process for the spore forming Bacillus spp . Our lab previously isolated and identified a bacterial strain Bacillus cereus tsu1. The bacterium was cultured on rapeseed cake substrate (RCS) and the maxima of PHB accumulation reached within 12 h, and depleted after 48 h; fore-spore and spore structure were observed after 24 h culture.Results Quantitative proteomic analysis of ‘ tsu1’ identified 3,215 proteins in total, out of which 2,952 got quantified. 244 were identified as significantly changed proteins (SCPs) in the 12-24-hour pair of samples, and 325 in the12-48-hour pair of samples. Gene Ontology classification revealed that enriched biological processes only found in the 12-24h pair SCPs include purine nucleotide metabolism, protein folding, metal ion homeostasis, response to stress, carboxylic acid catabolism, cellular amino acid catabolism; and those only found in the 12-48h pair SCPs were carbohydrate metabolism, protein metabolism, oxidative phosphorylation, formation of translation ternary structure. Based on statistical analysis, key enzymes poly(R)-hydroxyalkanoic acid synthase (PhaC, KGT44864) is significantly higher in 12h-culture; SigF, SpoEII related with sporulation were significantly higher in the 24h-samples; enzymes for nitrate respiration and fermentation were significantly induced in 48h-culture.Conclusions Proteome profile changes during PHB intracellular mobilization in B. cereus tsu1 were characterized in this study. The key enzyme PhaC for PHB synthesis is significantly higher in 12h-culture which supports the highest PHB accumulation at this time point; protein abundance of SpoIIE and σF were significantly increased to induce sporulation in 24h-culture; enzymes for nitrate respiration and fermentation were significantly induced in 48h-culture which implied the depletion of oxygen at this stage and carbon flow towards fermentative growth. The results from this study provide insights into proteome profile changes during PHB accumulation and reuse, which can be applied to achieve a higher PHB yield and to improve bacterial growth performance and stress resistance.

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“…The markerless gene deletion system based on the homing endonuclease I-SceI was established for B. thuringiensis, with procedures described in detail in our previous work (Zheng et al, 2015;Wang et al, 2016).…”

Section: Construction Of Deletion Mutants Of B Thuringiensismentioning

confidence: 99%

2‐Methylcitrate cycle: a well‐regulated controller of Bacillus sporulation

Cao

Du³

et al. 2019

Environmental Microbiology

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Summary Bacillus thuringiensis is the most widely used eco‐friendly biopesticide, containing two primary determinants of biocontrol, endospore and insecticidal crystal proteins (ICPs). The 2‐methylcitrate cycle is a widespread carbon metabolic pathway playing a crucial role in channelling propionyl‐CoA, but with poorly understood metabolic regulatory mechanisms. Here, we dissect the transcriptional regulation of the 2‐methylcitrate cycle operon prpCDB and report its unprecedented role in controlling the sporulation process of B. thuringiensis. We found that the transcriptional activity of the prp operon encoding the three critical enzymes PrpC, PrpD, and PrpB in the 2‐methylcitrate cycle was negatively regulated by the two global transcription factors CcpA and AbrB, while positively regulated by the LysR family regulator CcpC, which jointly account for the fact that the 2‐methylcitrate cycle is specifically and highly active in the stationary phase of growth. We also found that the prpD mutant accumulated 2‐methylcitrate, the intermediate metabolite of the 2‐methylcitrate cycle, which delayed and inhibited sporulation at the early stage. Thus, our results not only revealed sophisticated transcriptional regulatory mechanisms for the metabolic 2‐methylcitrate cycle but also identified 2‐methylcitrate as a novel regulator of sporulation in B. thuringiensis.

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Poly-β-hydroxybutyrate Metabolism Is Unrelated to the Sporulation and Parasporal Crystal Protein Formation in Bacillus thuringiensis

Cited by 17 publications

References 48 publications

Poly(3‐hydroxybutyrate) fuels the tricarboxylic acid cycle and de novo lipid biosynthesis during Bacillus anthracis sporulation

Poly(3‐hydroxybutyrate) fuels the tricarboxylic acid cycle and de novo lipid biosynthesis during Bacillus anthracis sporulation

Proteome Profile Changes During Poly-hydroxybutyrate Intracellular Mobilization in Gram Positive Bacillus cereus tsu1

2‐Methylcitrate cycle: a well‐regulated controller of Bacillus sporulation

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