<i>Bacillus subtilis</i> Lipid Extract, A Branched-Chain Fatty Acid Model Membrane

Nickels, Jonathan D.; Chatterjee, Sneha; Mostofian, Barmak; Stanley, Christopher B.; Ohl, Michael; Zolnierczuk, Piotr; Schulz, Roland; Myles, Dean A. A.; Standaert, Robert F.; Elkins, James G.; Cheng, Xiaolin; Katsaras, John

doi:10.1021/acs.jpclett.7b01877

Cited by 54 publications

(58 citation statements)

References 30 publications

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“…Comprehensive in vivo studies, however, have been difficult due to experimental challenges associated with modifying the fatty acid composition and, thus, membrane fluidity directly in growing cells. Consequently, our understanding of the behavior of biological membranes upon changing fluidity is predominately based on in vitro and in silico studies with simplified model lipids, or in vitro studies with either natural lipid extracts or isolated membranes (Baumgart et al, 2007;Nickels et al, 2017;Schäfer et al, 2011).…”

Section: Introductionmentioning

confidence: 99%

Low membrane fluidity triggers lipid phase separation and protein segregation in vivo

Gohrbandt

Lipski

Grimshaw

et al. 2019

Preprint

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Important physicochemical properties of cell membranes such as fluidity sensitively depend on fluctuating environmental factors including temperature, pH or diet. To counteract these disturbances, living cells universally adapt their lipid composition in return. In contrast to eukaryotic cells, bacteria tolerate surprisingly drastic changes in their lipid composition while retaining viability, thus making them a more tractable model to study this process. Using the model organisms Escherichia coli and Bacillus subtilis, which regulate their membrane fluidity with different fatty acid types, we show here that inadequate membrane fluidity interferes with essential cellular processes such as morphogenesis and maintenance of membrane potential, and triggers large-scale lipid phase separation that drives protein segregation into the fluid phase. These findings illustrate why lipid homeostasis is such a critical cellular process. Finally, our results provide direct in vivo support for current in vitro and in silico models regarding lipid phase separation and associated protein segregation.Keywords: Lipid phase separation, lipid domains, protein partitioning, membrane fluidity, homeoviscous adaptation, Escherichia coli, Bacillus subtilis, WALP, FOF1 ATP synthase liquid-disordered phase characterized by low packing density and high diffusion rates that forms the regular state of biological membranes, (ii) the more ordered, cholesterol/hopanoid-dependent liquidordered phase found in biological membranes in form of lipid rafts, and (iii) the gel phase characterized by dense lipid packing with little lateral or rotational diffusion, which is generally assumed to be absent in biologically active membranes (Schmid, 2017;Veatch, 2007). In fact, the temperature associated with gel phase formation has been postulated to define the lower end of the temperature range able to support vital cell functions (Burns et al., 2017;Drobnis et al., 1993;Ghetler et al., 2005). At last, the lipid phases can co-exist, resulting in separated membrane areas exhibiting distinctly different composition and characteristics (Baumgart et al., 2007;Elson et al., 2010;Heberle and Feigenson, 2011). This principal mechanism of lipid domain formation is best studied in the context of lipid rafts (Lingwood and Simons, 2010).While in vitro and in silico approaches with simplified lipid models have provided detailed insights into the complex physicochemical behavior of lipid bilayers, testing the formed hypotheses and models in the context of protein-rich biological membranes is now crucial. Bacteria tolerate surprisingly drastic changes in their lipid composition and only possess one or two membrane layers as part of their cell envelope. Consequently, bacteria are both a suitable and a more tractable model to study the fundamental biological process linked to membrane fluidity and phase separation in vivo.We analyzed the biological importance of membrane homeoviscous adaptation in Escherichia coli (phylum Proteobacteria) and Bacillus subtilis (phylum Firmic...

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Section: Introductionmentioning

confidence: 99%

Low membrane fluidity triggers lipid phase separation and protein segregation in vivo

Gohrbandt

Lipski

Grimshaw

et al. 2019

Preprint

View full text Add to dashboard Cite

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“…A comparison of melting temperatures for lipids with PE vs. PG headgroups, but the same FAs illustrates this phenomenon [1,2-dipalmitoyl-snglycero-3-phosphoethanolamine (DPPE; PE32:0) has a Tm of 63 • C vs. 1,2-dipalmitoyl-sn-glycero-3-phosphoglycerol (DPPG; PG32:0) which has a Tm of 41 • C] (Tm tabulated at avantipolarlipids.com). The native cell membrane of B. subtilis 168 contains PE, PG, cardiolipin (CL), and lysyl-PG lipids, in addition to ∼30 percent neutral lipids which are mostly diacylglycerol (Bishop et al, 1967;Den Kamp et al, 1969;Clejan et al, 1986;Kawai et al, 2004;Nickels et al, 2017a; Figure 5A). In the labeled cells, the substantial decrease in PE, and corresponding increase in PG, would have a fluidizing effect upon the membrane, potentially counteracting the ordering effect of increasing n16:0 FA content.…”

Section: Resultsmentioning

confidence: 99%

Impact of Fatty-Acid Labeling of Bacillus subtilis Membranes on the Cellular Lipidome and Proteome

et al. 2020

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“…The various functions of different types of FAs in terms of environmental responses are due to their diverse structures as summarized in Table 2. FAs compositions in the genus Bacillus in general and in B. megaterium species in particular are characterized by numerous branched-chain FAs (BCFAs), with a predominance of iso and anteiso BCFAs composed of 14-17 carbons, and smaller amounts of straight chain FAs (Kaneda 1966(Kaneda , 1977Choi et al 2000;Nickels et al 2017a, b). However, an opposite scenario, with low ratios of BCFAs/SCFAs and SFAs/USFAs, was found in TCDD-exposed bacteria (Hanano et al 2019b).…”

Section: Effects Of Dioxins On Lipid Metabolism In Soil Microorganismsmentioning

confidence: 99%

Dioxin impacts on lipid metabolism of soil microbes: towards effective detection and bioassessment strategies

Mahfouz

Mansour

Murphy

et al. 2020

Bioresour. Bioprocess.

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Dioxins are the most toxic known environmental pollutants and are mainly formed by human activities. Due to their structural stability, dioxins persist for extended periods and can be transported over long distances from their emission sources. Thus, dioxins can be accumulated to considerable levels in both human and animal food chains. Along with sediments, soils are considered the most important reservoirs of dioxins. Soil microorganisms are therefore highly exposed to dioxins, leading to a range of biological responses that can impact the diversity, genetics and functional of such microbial communities. Dioxins are very hydrophobic with a high affinity to lipidic macromolecules in exposed organisms, including microbes. This review summarizes the genetic, molecular and biochemical impacts of dioxins on the lipid metabolism of soil microbial communities and especially examines modifications in the composition and architecture of cell membranes. This will provide a useful scientific benchmark for future attempts at soil ecological risk assessment, as well as in identifying potential dioxin-specific-responsive lipid biomarkers. Finally, potential uses of lipid-sequestering microorganisms as a part of biotechnological approaches to the bio-management of environmental contamination with dioxins are discussed.

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Bacillus subtilis Lipid Extract, A Branched-Chain Fatty Acid Model Membrane

Cited by 54 publications

References 30 publications

Low membrane fluidity triggers lipid phase separation and protein segregation in vivo

Low membrane fluidity triggers lipid phase separation and protein segregation in vivo

Impact of Fatty-Acid Labeling of Bacillus subtilis Membranes on the Cellular Lipidome and Proteome

Dioxin impacts on lipid metabolism of soil microbes: towards effective detection and bioassessment strategies

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