Metabolic control of the membrane fluidity in Bacillus subtilis during cold adaptation

Beranová, Jana; Jemioła-Rzemińska, Małgorzata; Elhottová, Dana; Strzałka, Kazimierz; Konopásek, Ivo

doi:10.1016/j.bbamem.2007.11.012

Cited by 54 publications

(47 citation statements)

References 24 publications

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“…(ii) Fluorescence anisotropy. Fluorescence anisotropy with 1,6-diphenyl-1,3,5-hexatriene (DPH), which is used to represent global membrane fluidity (5,10,45), was measured at test temperatures of 5, 18, and 39°C on cells from aerobic and anaerobic cultures grown at 15 and 37°C (Fig. 5).…”

Section: Membrane Properties (I) Ft-ir Spectroscopymentioning

confidence: 99%

Influence of Anaerobiosis and Low Temperature on Bacillus cereus Growth, Metabolism, and Membrane Properties

Sarrau

Clavel

Clerté

et al. 2012

Appl Environ Microbiol

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The impact of simultaneous anaerobiosis and low temperature on growth parameters, metabolism, and membrane properties of Bacillus cereus ATCC 14579 was studied. No growth was observed under anaerobiosis at 12°C. In bioreactors, growth rates and biomass production were drastically reduced by simultaneous anaerobiosis and low temperature (15°C). The two conditions had a synergistic effect on biomass reduction. In anaerobic cultures, fermentative metabolism was modified by low temperature, with a marked reduction in ethanol production leading to a lower ability to produce NAD ؉ . Anaerobiosis reduced unsaturated fatty acids at both low optimal temperatures. In addition, simultaneous anaerobiosis and low temperatures markedly reduced levels of branched-chain fatty acids compared to all other conditions (accounting for 33% of total fatty acids against more 71% for low-temperature aerobiosis, optimal-temperature aerobiosis, and optimal-temperature anaerobiosis). This corresponded to high-melting-temperature lipids and to low-fluidity membranes, as indicated by differential scanning calorimetry, 1,6-diphenyl-1,3,5-hexatriene (DPH) fluorescence anisotropy, and infrared spectroscopy. This is in contrast to requirements for cold adaptation. A link between modification in the synthesis of metabolites of fermentative metabolism and the reduction of branchedchain fatty acids at low temperature under anaerobiosis, through a modification of the oxidizing capacity, is assumed. This link may partly explain the impact of low temperature and anaerobiosis on membrane properties and growth performance.

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Section: Membrane Properties (I) Ft-ir Spectroscopymentioning

confidence: 99%

Influence of Anaerobiosis and Low Temperature on Bacillus cereus Growth, Metabolism, and Membrane Properties

Sarrau

Clavel

Clerté

et al. 2012

Appl Environ Microbiol

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“…DPH fluorescence anisotropy (r ss ) was then measured over the temperature range of 5°C to 45°C. The protocols used have been detailed in our previous work (5).…”

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confidence: 99%

“…Individual FA peaks were identified using the automatic identification system (MIDI Inc.). Detailed procedures have been described in our previous paper (5).…”

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confidence: 99%

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Differences in Cold Adaptation of Bacillus subtilis under Anaerobic and Aerobic Conditions

et al. 2010

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Bacillus subtilis, which grows under aerobic conditions, employs fatty acid desaturase (Des) to fluidize its membrane when subjected to temperature downshift. Des requires molecular oxygen for its activity, and its expression is regulated by DesK-DesR, a two-component system. Transcription of des is induced by the temperature downshift and is decreased when membrane fluidity is restored. B. subtilis is also capable of anaerobic growth by nitrate or nitrite respiration. We studied the mechanism of cold adaptation in B. subtilis under anaerobic conditions that were predicted to inhibit Des activity. We found that in anaerobiosis, in contrast to aerobic growth, the induction of des expression after temperature downshift (from 37°C to 25°C) was not downregulated. However, the transfer from anaerobic to aerobic conditions rapidly restored the downregulation. Under both aerobic and anaerobic conditions, the induction of des expression was substantially reduced by the addition of external fluidizing oleic acid and was fully dependent on the DesK-DesR twocomponent regulatory system. Fatty acid analysis proved that there was no desaturation after des induction under anaerobic conditions despite the presence of high levels of the des protein product, which was shown by immunoblot analysis. The cold adaptation of B. subtilis in anaerobiosis is therefore mediated exclusively by the increased anteiso/iso ratio of branched-chain fatty acids and not by the temporarily increased level of unsaturated fatty acids that is typical under aerobic conditions. The degrees of membrane fluidization, as measured by diphenylhexatriene fluorescence anisotropy, were found to be similar under both aerobic and anaerobic conditions.Bacterial growth requires an appreciable fraction of the acyl chains of the membrane lipids to be in a disordered state. Such disordered states are brought about by fatty acids that act to offset the closely packed ordered arrangement of the lipid bilayer acyl chains that are imparted by the straight-chain saturated acyl chains. In most bacteria, the role of introducing acyl chain disorder is fulfilled by unsaturated fatty acids. Some bacteria synthesize UFAs by the process of desaturation, an oxygen-requiring reaction that introduces the double bond into a single concerted reaction. However, this is not an option for bacteria that grow under anaerobic conditions. For example, in the upper layers of soil, which are the natural habitat of Bacillus subtilis, the fluctuations in oxygen availability that are mostly caused by the changing water content are common.Even though B. subtilis is still generally considered to be an obligate aerobe, several recent studies have proved that this bacterium is in fact a facultative anaerobe, which is capable of both fermentation and anaerobic respiration with either nitrate or nitrite used as the terminal electron acceptor (19,20). The key role in the complex regulation of anaerobic metabolism of B. subtilis can be attributed to the genes resD and resE (21, 26) and fnr (23).A decreas...

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“…Growth at low temperatures can lead to changes in membrane composition (4,23) that could affect the type and density of functional groups present on the cell surface. In addition to changes in fatty acid composition and carotenoid content, Corsaro et al (12) observed an increase in phosphorylation of lipooligosaccharides and exopolysaccharides with an increase in growth temperature for Pseudoalteromonas haloplanktis, an Antarctic bacterium.…”

Section: Downloaded Frommentioning

confidence: 99%

Role of Extracellular Polymeric Substances in the Surface Chemical Reactivity of Hymenobacter aerophilus , a Psychrotolerant Bacterium

Baker

Lalonde

Konhauser

et al. 2010

Appl Environ Microbiol

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Bacterial surface layers, such as extracellular polymeric substances (EPS), are known to play an important role in metal sorption and biomineralization; however, there have been very few studies investigating how environmentally induced changes in EPS production affect the cell's surface chemistry and reactivity. Acidbase titrations, cadmium adsorption assays, and Fourier transform infrared spectroscopy (FT-IR) were used to characterize the surface reactivities of Hymenobacter aerophilus cells with intact EPS (WC) or stripped of EPS (SC) and purified EPS alone. Linear programming modeling of titration data showed SC to possess functional groups corresponding to phosphoryl (pK a ϳ6.5), phosphoryl/amine (pK a ϳ7.9), and amine/hydroxyl (pK a ϳ9.9). EPS and WC both possess carboxyl groups (pK a ϳ5.1 to 5.8) in addition to phosphoryl and amine groups. FT-IR confirmed the presence of polysaccharides and protein in purified EPS that can account for the additional carboxyl groups. An increased ligand density was observed for WC relative to that for SC, leading to an increase in the amount of Cd adsorbed (0.53 to 1.73 mmol/liter per g [dry weight] and 0.53 to 0.59 mmol/liter per g [dry weight], respectively). Overall, the presence of EPS corresponds to an increase in the number and type of functional groups on the surface of H. aerophilus that is reflected by increased metal adsorption relative to that for EPS-free cells.Acid-base titrations are frequently used to characterize microbial cell surface reactivity, in particular, the ability of the cell to adsorb and desorb protons (19,21,47). This ability is conferred by the presence of proton-reactive surface functional groups that are also responsible for the surface adsorption of other cations, including dissolved metals. Thus, a microbe's ability to immobilize metals and influence metal transport is largely dependent on the nature of the reactive sites found at the cell-water interface, namely, their concentrations and chemical affinities (in terms of equilibrium surface stability constants) for cations such as protons and metals.Both Gram-negative and Gram-positive bacteria have been characterized extensively using acid-base titration to determine their reactivity with respect to geochemical processes (18,22,33). To date, most work has focused on mesophilic and strictly heterotrophic model organisms; however, some work has also been done with cyanobacteria (29, 44) and thermophiles (19,47). While proton sorption assays provide information on surface site densities and acidity constants, a more direct assessment of a microbe's ability to interact with aqueous metals is the metal adsorption assay, where a cell's ability to adsorb metal ions from solution is measured over a range of pH values. Metal adsorption assays have been used to characterize microbes from a wide variety of environments to determine their potential for bioremediation of heavy metal contamination (21, 26), their influence on geochemical cycling (5, 16), and their ability to serve as nucleation sites f...

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Metabolic control of the membrane fluidity in Bacillus subtilis during cold adaptation

Cited by 54 publications

References 24 publications

Influence of Anaerobiosis and Low Temperature on Bacillus cereus Growth, Metabolism, and Membrane Properties

Influence of Anaerobiosis and Low Temperature on Bacillus cereus Growth, Metabolism, and Membrane Properties

Differences in Cold Adaptation of Bacillus subtilis under Anaerobic and Aerobic Conditions

Role of Extracellular Polymeric Substances in the Surface Chemical Reactivity of Hymenobacter aerophilus , a Psychrotolerant Bacterium

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