Membrane Vesicle Formation as a Multiple-Stress Response Mechanism Enhances Pseudomonas putida DOT-T1E Cell Surface Hydrophobicity and Biofilm Formation

Baumgarten, Thomas; Sperling, Stefanie; Seifert, Jana; Bergen, Martin von; Steiniger, Frank; Wick, Lukas Y.; Heipieper, Hermann J.

doi:10.1128/aem.01525-12

Cited by 220 publications

(206 citation statements)

References 46 publications

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“…The different responses to changes in pH, ionic strength, and storage in the MATH assay versus filter columns show that the mechanism of adherence to hydrocarbons (in this case, hexadecane) and quartz sand is not the same and that the MATH assay cannot be used solely to predict adhesion behavior in sand. Furthermore, it was recently shown that gram-negative bacteria release membrane vesicles as a stress response changing the surface properties of the cells, including their hydrophobicity and tendency to form biofilm (Baumgarten et al 2012). Especially, the change from growth medium to various NaCl solutions (experiment 3) may have induced stress responses contributing to the nonobvious relationship between ionic strength and adhesion to quartz sand.…”

Section: Discussionmentioning

confidence: 99%

Using 2,6-dichlorobenzamide (BAM) degrading Aminobacter sp. MSH1 in flow through biofilters—initial adhesion and BAM degradation potentials

Albers

Jacobsen

Aamand

2013

Appl Microbiol Biotechnol

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Micropollutants in groundwater are given significant attention by water companies and authorities due to an increasing awareness that they might be present even above the legal threshold values. As part of our investigations of the possibility to remove the common groundwater pollutant 2,6-dichlorobenzamide (BAM) by introducing the efficient BAM degrader Aminobacter sp. MSH1 into biologically active sand filters, we investigated if the strain adheres to filters containing various filter materials and if the initial adherence and subsequent degradation of BAM could be optimized. We found that most of the inoculated MSH1 cells adhered fast and that parameters like pH and ionic strength had only a minor influence on the adhesion despite huge influence on cell surface hydrophobicity. At the given growth protocol, the MSH1 strain apparently developed a subpopulation that had lost its ability to adhere to the filter materials, which was supported by attempted reinoculation of non-adhered cells. Analysis by quantitative PCR showed that most cells adhered in the top of the filters and that some of these were lost from the filters during initial operation, while insignificant losses occurred after 1 day of operation. The inoculated filters were found to degrade 2.7 μg/L BAM to below 0.1 μg/L at a 1.1-h residence time with insignificant formation of known degradation products. In conclusion, most filter materials and water types should be feasible for inoculation with the MSH1 strain, while more research into degradation at low concentrations and temperatures is needed before this technology is ready for use at actual waterworks.

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Section: Discussionmentioning

confidence: 99%

Using 2,6-dichlorobenzamide (BAM) degrading Aminobacter sp. MSH1 in flow through biofilters—initial adhesion and BAM degradation potentials

Albers

Jacobsen

Aamand

2013

Appl Microbiol Biotechnol

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“…S1 and Table S3 in the supplemental material) in C. beijerinckii NCIMB 8052 cells grown in the presence of CaCO 3 , even though samples for protein extraction were taken at the same butanol concentration for both treated and control cultures. Finally, while several genetic and biochemical factors dictate biofilm formation, solvent stress is a positive effector (76); in this regard, it is notable that C. beijerinckii cells grown in the presence of CaCO 3 showed 5-and 2-fold decreases in levels of polysaccharide deacetylase and diguanylate cyclase, respectively (see Fig. S1 and Table S3 in the supplemental material), two enzymes that facilitate biofilm formation due to their roles in exopolysaccharide deacetylation and the generation of the bis-(3=-5=)-cyclic dimeric GMP (c-di-GMP) biofilm-signaling molecule, respectively (77).…”

Section: Discussionmentioning

confidence: 99%

Use of Proteomic Analysis To Elucidate the Role of Calcium in Acetone-Butanol-Ethanol Fermentation by Clostridium beijerinckii NCIMB 8052

Han

Ujor

Lai

et al. 2013

Appl Environ Microbiol

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c Calcium carbonate increases growth, substrate utilization, and acetone-butanol-ethanol (ABE) fermentation by Clostridium beijerinckii NCIMB 8052. Toward an understanding of the basis for these pleiotropic effects, we profiled changes in the C. beijerinckii NCIMB 8052 proteome that occur in response to the addition of CaCO 3 . We observed increases in the levels of different heat shock proteins (GrpE and DnaK), sugar transporters, and proteins involved in DNA synthesis, repair, recombination, and replication. We also noted significant decreases in the levels of proteins involved in metabolism, nucleic acid stabilization, sporulation, oxidative and antibiotic stress responses, and signal transduction. We determined that CaCO 3 enhances ABE fermentation due to both its buffering effects and its ability to influence key cellular processes, such as sugar transport, butanol tolerance, and solventogenesis. Moreover, activity assays in vitro for select solventogenic enzymes revealed that part of the underpinning for the CaCO 3 -mediated increase in the level of ABE fermentation stems from the enhanced activity of these catalysts in the presence of Ca 2؉ . Collectively, these proteomic and biochemical studies provide new insights into the multifactorial basis for the stimulation of ABE fermentation and butanol tolerance in the presence of CaCO 3 . Growing concerns over increased emissions of greenhouse gases from the combustion of fossil fuels and the global energy crisis have recently spawned extensive research into renewable energy. As a result, there is a resurgent interest in butanol as an alternative fuel, due mainly to its higher energy content than ethanol and its compatibility with gasoline, with the latter trait making it more compatible with existing pipelines for distribution (1, 2). However, the cost of butanol production, which currently relies on petroleum feedstock, is not favorable compared to gasoline (3). Although acetone-butanol-ethanol (ABE) fermentation with solventogenic Clostridium species holds promise as a potentially cheaper means of butanol production, low yields and productivity due to butanol toxicity to the fermenting cells have hampered the commercialization of biobutanol (4, 5).To increase yield and productivity, fermentation broth additives such as acetate (6, 7) and calcium carbonate (3, 8, 9) have been successfully utilized. During ABE fermentation by solventogenic Clostridium species, CaCO 3 has been shown to stimulate sugar utilization, butanol production, and butanol tolerance (3,8,9). For example, during Clostridium acetobutylicum fermentation, the addition of 8 g/liter butanol (to mimic solvent intolerance) limited xylose utilization to 30 g/liter (from a starting concentration of 60 g/liter); however, upon the addition of CaCO 3 (10 g/liter), xylose utilization increased to 43 g/liter (8). Similarly, when ABE fermentation was conducted in an iron-deficient medium, which modifies carbon and electron flow to favor early butanol accumulation, the xylose utilization by C. acetobutyl...

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“…They are also involved in the transport of metabolites, toxins, signalling molecules and other small molecules (Horstman & Kuehn, 2000Dutta et al, 2004;Keenan et al, 2008;Bomberger et al, 2009;Schertzer & Whiteley, 2012;Biller et al, 2014;Klimentová & Stulík, 2015). Furthermore, the formation of OMVs is a crucial part of the bacterial envelope stress response, protecting the bacteria from internal and external stressors (Manning & Kuehn, 2011;Baumgarten et al, 2012;MacDonald & Kuehn, 2012;Schwechheimer et al, 2013Schwechheimer et al, , 2014. In the present study, we investigated the formation of OMVs in P. putida A (ATCC 12633) in the presence of the QAC TTAB.…”

Section: Introductionmentioning

confidence: 98%

Release of outer membrane vesicles in Pseudomonas putida as a response to stress caused by cationic surfactants

et al. 2016

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Release of outer membrane vesicles inPseudomonas putida A (ATCC 12633), a degrader of cationic surfactants, releases outer membrane vesicles (OMVs) when grown with tetradecyltrimethylammonium bromide (TTAB) as the sole carbon, nitrogen and energy source. The OMVs exhibit a bilayer structure and were found to be composed of lipopolysaccharides, proteins and phospholipids (PLs) such as cardiolipin, phosphatidylcholine, phosphatidic acid and phosphatidylglycerol (PG). The OMVs showed a marked increase in the PG content, approximately 43 % higher than the amount registered in the parent cells from which the vesicles were derived. After growth of P. putida with TTAB, the amount of lipoprotein covalently cross-linked to the peptidoglycan showed a twofold decrease when compared with values found after growth without the surfactant [16¡2 and 28¡3 mg (mg cell envelope protein) 21, respectively]. This decrease in the amount of lipoprotein can be related to areas of loss of contact between the outer membrane and the peptidoglycan and, therefore, to OMV production. In addition, due to its amphiphilic nature, TTAB can contribute to OMV biogenesis, through a physical mechanism, by induction of the curvature of the membrane. Taking into account that OVMs were produced when the cells were grown under external stress, caused by the surfactant, and that TTAB was detected in the vesicles [48 nmol TTAB (nmol PL) 21], we concluded that this system of TTAB elimination is a mechanism that P. putida A (ATCC 12633) would utilize for alleviating stress caused by cationic surfactants.

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Membrane Vesicle Formation as a Multiple-Stress Response Mechanism Enhances Pseudomonas putida DOT-T1E Cell Surface Hydrophobicity and Biofilm Formation

Cited by 220 publications

References 46 publications

Using 2,6-dichlorobenzamide (BAM) degrading Aminobacter sp. MSH1 in flow through biofilters—initial adhesion and BAM degradation potentials

Using 2,6-dichlorobenzamide (BAM) degrading Aminobacter sp. MSH1 in flow through biofilters—initial adhesion and BAM degradation potentials

Use of Proteomic Analysis To Elucidate the Role of Calcium in Acetone-Butanol-Ethanol Fermentation by Clostridium beijerinckii NCIMB 8052

Release of outer membrane vesicles in Pseudomonas putida as a response to stress caused by cationic surfactants

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