scholarly journals Changes in the distribution of membrane lipids during growth of Thermotoga maritima at different temperatures: Indications for the potential mechanism of biosynthesis of ether-bound diabolic acid (membrane-spanning) lipids

2021 ◽  
Author(s):  
Diana X. Sahonero-Canavesi ◽  
Laura Villanueva ◽  
Nicole J. Bale ◽  
Jade Bosviel ◽  
Michel Koenen ◽  
...  
Keyword(s):  
Membrane Lipids ◽  
Lipid Analysis ◽  
Thermotoga Maritima ◽  
Lipid Level ◽  
Condensation Reaction ◽  
Physiological Role ◽  
Dicarboxylic Acids ◽  
Protein Domain ◽  
Alkyl Ether ◽  
Membrane Spanning

Membrane-spanning lipids are present in a wide variety of archaea but they are rarely in bacteria. Nevertheless, the (hyper)thermophilic members of the order Thermotogales harbor tetraester, tetraether, and mixed ether/ester membrane-spanning lipids mostly composed of core lipids derived from diabolic acids, C 30, C 32 and C 34 dicarboxylic acids with two adjacent mid-chain methyl substituents. Lipid analysis of Thermotoga maritima across growth phases revealed a decrease of the relative abundance of fatty acids together with an increase of diabolic acids with independence of growth temperature. We also identified isomers of C 30 and C 32 diabolic acids, i.e. dicarboxylic acids with only one methyl group at C-15. Their distribution suggests they are products of the condensation reaction but preferably produced when the length of the acyl chains is not optimal. In comparison with growth at the optimal temperature of 80°C, an increase of glycerol ether-derived lipids was observed at 55°C. Besides, our analysis only detected diabolic acid-containing intact polar lipids with phosphoglycerol (PG) headgroups. Considering these findings, we hypothesize a biosynthetic pathway for the synthesis of membrane-spanning lipids based on PG polar lipid formation, suggesting that the protein catalyzing this process could be a membrane protein. We also identified, by genomic and protein domain analyses, a gene coding for a putative plasmalogen synthase homologue in T. maritima , which is also present in other bacteria producing sn 1-alkyl ether lipids but not plasmalogens, suggesting it could be involved in the conversion of the ester to ether bond in the diabolic acids bound in membrane-spanning lipids. Importance Membrane-spanning lipids are unique compounds found in most archaeal membranes, but they are also present in specific bacterial groups like the Thermotogales. The synthesis and physiological role of membrane-spanning lipids in bacteria represent an evolutionary and biochemical open question that points to the differentiation of the membrane lipids composition. Understanding the formation of membrane-spanning lipids is crucial to solving this question and identifying the enzymatic and biochemical mechanism performing this procedure. In the present work, we found changes at the core lipid level, and we propose that the growth phase drives the biosynthesis of these lipids rather than temperature. Our results identified physiological conditions influencing the membrane-spanning lipids biosynthetic process which can further clarify the pathway leading to the biosynthesis of these compounds.

scholarly journals Calditol-linked membrane lipids are required for acid tolerance inSulfolobus acidocaldarius

2018 ◽  
Vol 115 (51) ◽  
pp. 12932-12937 ◽  
Author(s):  
Zhirui Zeng ◽  
Xiao-Lei Liu ◽  
Jeremy H. Wei ◽  
Roger E. Summons ◽  
Paula V. Welander
Keyword(s):  
Membrane Lipids ◽  
Phylogenetic Analyses ◽  
Critical Role ◽  
Extreme Temperature ◽  
Physiological Role ◽  
Acid Tolerance ◽  
Head Group ◽  
Ring Structures ◽  
Membrane Spanning ◽  
Archaeal Lipids

Archaea have many unique physiological features of which the lipid composition of their cellular membranes is the most striking. Archaeal ether-linked isoprenoidal membranes can occur as bilayers or monolayers, possess diverse polar head groups, and a multiplicity of ring structures in the isoprenoidal cores. These lipid structures are proposed to provide protection from the extreme temperature, pH, salinity, and nutrient-starved conditions that many archaea inhabit. However, many questions remain regarding the synthesis and physiological role of some of the more complex archaeal lipids. In this study, we identify a radicalS-adenosylmethionine (SAM) protein inSulfolobus acidocaldariusrequired for the synthesis of a unique cyclopentyl head group, known as calditol. Calditol-linked glycerol dibiphytanyl glycerol tetraethers (GDGTs) are membrane spanning lipids in which calditol is ether bonded to the glycerol backbone and whose production is restricted to a subset of thermoacidophilic archaea of the Sulfolobales order within the Crenarchaeota phylum. Several studies have focused on the enzymatic mechanism for the synthesis of the calditol moiety, but to date no protein that catalyzes this reaction has been discovered. Phylogenetic analyses of this putative calditol synthase (Cds) reveal the genetic potential for calditol–GDGT synthesis in phyla other than the Crenarchaeota, including the Korarchaeota and Marsarchaeota. In addition, we identify Cds homologs in metagenomes predominantly from acidic ecosystems. Finally, we demonstrate that deletion of calditol synthesis rendersS. acidocaldariussensitive to extremely low pH, indicating that calditol plays a critical role in protecting archaeal cells from acidic stress.

scholarly journals Lipidomics Provides New Insight into Pathogenesis and Therapeutic Targets of the Ischemia—Reperfusion Injury

2021 ◽  
Vol 22 (6) ◽  
pp. 2798
Author(s):  
Zoran Todorović ◽  
Siniša Đurašević ◽  
Maja Stojković ◽  
Ilijana Grigorov ◽  
Slađan Pavlović ◽  
...  
Keyword(s):  
Fatty Acids ◽  
Time Course ◽  
Membrane Lipids ◽  
Lipid Analysis ◽  
Cell Damage ◽  
Ischemia Reperfusion ◽  
Enzyme Inactivation ◽  
Critical Event ◽  
Tissue Ischemia ◽  
Insight Into

Lipids play an essential role in both tissue protection and damage. Tissue ischemia creates anaerobic conditions in which enzyme inactivation occurs, and reperfusion can initiate oxidative stress that leads to harmful changes in membrane lipids, the formation of aldehydes, and chain damage until cell death. The critical event in such a series of harmful events in the cell is the unwanted accumulation of fatty acids that leads to lipotoxicity. Lipid analysis provides additional insight into the pathogenesis of ischemia/reperfusion (I/R) disorders and reveals new targets for drug action. The profile of changes in the composition of fatty acids in the cell, as well as the time course of these changes, indicate both the mechanism of damage and new therapeutic possibilities. A therapeutic approach to reperfusion lipotoxicity involves attenuation of fatty acids overload, i.e., their transport to adipose tissue and/or inhibition of the adverse effects of fatty acids on cell damage and death. The latter option involves using PPAR agonists and drugs that modulate the transport of fatty acids via carnitine into the interior of the mitochondria or the redirection of long-chain fatty acids to peroxisomes.

scholarly journals Biochemical characterisation of four rhamnosidases from thermophilic bacteria of the genera Thermotoga, Caldicellulosiruptor and Thermoclostridium

2019 ◽  
Vol 9 (1) ◽  
Author(s):  
Melanie Baudrexl ◽  
Wolfgang H. Schwarz ◽  
Vladimir V. Zverlov ◽  
Wolfgang Liebl
Keyword(s):  
Thermophilic Bacteria ◽  
Thermotoga Maritima ◽  
Physiological Role ◽  
Structural Similarity ◽  
Glycoside Hydrolase Family ◽  
Thermotoga Neapolitana ◽  
Cobalt Nickel ◽  
Biochemical Characterisation ◽  
Hydrolase Family ◽  
Nickel Manganese

Abstract Carbohydrate active enzymes are classified in databases based on sequence and structural similarity. However, their function can vary considerably within a similarity-based enzyme family, which makes biochemical characterisation indispensable to unravel their physiological role and to arrive at a meaningful annotation of the corresponding genes. In this study, we biochemically characterised the four related enzymes Tm_Ram106B, Tn_Ram106B, Cb_Ram106B and Ts_Ram106B from the thermophilic bacteria Thermotoga maritima MSB8, Thermotoga neapolitana Z2706-MC24, Caldicellulosiruptor bescii DSM 6725 and Thermoclostridium stercorarium DSM 8532, respectively, as α-l-rhamnosidases. Cobalt, nickel, manganese and magnesium ions stimulated while EDTA and EGTA inhibited all four enzymes. The kinetic parameters such as Km, Vmax and kcat were about average compared to other rhamnosidases. The enzymes were inhibited by rhamnose, with half-maximal inhibitory concentrations (IC50) between 5 mM and 8 mM. The α-l-rhamnosidases removed the terminal rhamnose moiety from the rutinoside in naringin, a natural flavonone glycoside. The Thermotoga sp. enzymes displayed the highest optimum temperatures and thermostabilities of all rhamnosidases reported to date. The four thermophilic and divalent ion-dependent rhamnosidases are the first biochemically characterised orthologous enzymes recently assigned to glycoside hydrolase family 106.

scholarly journals Adaptive Evolution of Thermotoga maritima Reveals Plasticity of the ABC Transporter Network

2015 ◽  
Vol 81 (16) ◽  
pp. 5477-5485 ◽  
Author(s):  
Haythem Latif ◽  
Merve Sahin ◽  
Janna Tarasova ◽  
Yekaterina Tarasova ◽  
Vasiliy A. Portnoy ◽  
...  
Keyword(s):  
Abc Transporter ◽  
Abc Transporters ◽  
Thermotoga Maritima ◽  
Binding Protein ◽  
Carbon Sources ◽  
Peptide Transport ◽  
Content Type ◽  
Upstream Promoter ◽  
Membrane Spanning ◽  
Vast Network

ABSTRACTThermotoga maritimais a hyperthermophilic anaerobe that utilizes a vast network of ABC transporters to efficiently metabolize a variety of carbon sources to produce hydrogen. For unknown reasons, this organism does not metabolize glucose as readily as it does glucose di- and polysaccharides. The leading hypothesis implicates the thermolability of glucose at the physiological temperatures at whichT. maritimalives. After a 25-day laboratory evolution, phenotypes were observed with growth rates up to 1.4 times higher than and glucose utilization rates exceeding 50% those of the wild type. Genome resequencing revealed mutations in evolved cultures related to glucose-responsive ABC transporters. The native glucose ABC transporter, GluEFK, has more abundant transcripts either as a result of gene duplication-amplification or through mutations to the operator sequence regulating this operon. Conversely, BglEFGKL, a transporter of beta-glucosides, is substantially downregulated due to a nonsense mutation to the solute binding protein or due to a deletion of the upstream promoter. Analysis of the ABC2 uptake porter families for carbohydrate and peptide transport revealed that the solute binding protein, often among the transcripts detected at the highest levels, is predominantly downregulated in the evolved cultures, while the membrane-spanning domain and nucleotide binding components are less varied. Similar trends were observed in evolved strains grown on glycerol, a substrate that is not dependent on ABC transporters. Therefore, improved growth on glucose is achieved through mutations favoring GluEFK expression over BglEFGKL, and in lieu of carbon catabolite repression, the ABC transporter network is modulated to achieve improved growth fitness.

Cyclopropane ring formation in membrane lipids of bacteria

1997 ◽  
Vol 61 (4) ◽  
pp. 429-441 ◽  
Author(s):  
D W Grogan ◽  
J E Cronan
Keyword(s):  
Fatty Acids ◽  
Double Bond ◽  
Lipid Bilayers ◽  
Unsaturated Fatty Acids ◽  
Membrane Lipids ◽  
Cyclopropane Ring ◽  
Saturated Fatty Acids ◽  
Physiological Role ◽  
Phospholipid Bilayer ◽  
Valuable Insight

It has been known for several decades that cyclopropane fatty acids (CFAs) occur in the phospholipids of many species of bacteria. CFAs are formed by the addition of a methylene group, derived from the methyl group of S-adenosylmethionine, across the carbon-carbon double bond of unsaturated fatty acids (UFAs). The C1 transfer does not involve free fatty acids or intermediates of phospholipid biosynthesis but, rather, mature phospholipid molecules already incorporated into membrane bilayers. Furthermore, CFAs are typically produced at the onset of the stationary phase in bacterial cultures. CFA formation can thus be considered a conditional, postsynthetic modification of bacterial membrane lipid bilayers. This modification is noteworthy in several respects. It is catalyzed by a soluble enzyme, although one of the substrates, the UFA double bond, is normally sequestered deep within the hydrophobic interior of the phospholipid bilayer. The enzyme, CFA synthase, discriminates between phospholipid vesicles containing only saturated fatty acids and those containing UFAs; it exhibits no affinity for vesicles of the former composition. These and other properties imply that topologically novel protein-lipid interactions occur in the biosynthesis of CFAs. The timing and extent of the UFA-to-CFA conversion in batch cultures and the widespread distribution of CFA synthesis among bacteria would seem to suggest an important physiological role for this phenomenon, yet its rationale remains unclear despite experimental tests of a variety of hypotheses. Manipulation of the CFA synthase of Escherichia coli by genetic methods has nevertheless provided valuable insight into the physiology of CFA formation. It has identified the CFA synthase gene as one of several rpoS-regulated genes of E. coli and has provided for the construction of strains in which proposed cellular functions of CFAs can be properly evaluated. Cloning and manipulation of the CFA synthase structural gene have also enabled this novel but extremely unstable enzyme to be purified and analyzed in molecular terms and have led to the identification of mechanistically related enzymes in clinically important bacterial pathogens.

scholarly journals Lipid Synthetic Transcription Factor SREBP-1a Activates p21WAF1/CIP1, a Universal Cyclin-Dependent Kinase Inhibitor

2005 ◽  
Vol 25 (20) ◽  
pp. 8938-8947 ◽  
Author(s):  
Noriyuki Inoue ◽  
Hitoshi Shimano ◽  
Masanori Nakakuki ◽  
Takashi Matsuzaka ◽  
Yoshimi Nakagawa ◽  
...  
Keyword(s):  
Cell Growth ◽  
Kinase Inhibitor ◽  
Membrane Lipids ◽  
Regulatory Element ◽  
Lipid Synthesis ◽  
Physiological Role ◽  
Cyclin Dependent Kinase ◽  
New Paradigm ◽  
Protein Levels ◽  
Cyclin Dependent Kinase Inhibitor

ABSTRACT Sterol regulatory element-binding proteins (SREBPs) are membrane-bound transcription factors that regulate lipid synthetic genes. In contrast to SREBP-2, which regulates cellular cholesterol level in normal cells, SREBP-1a is highly expressed in actively growing cells and activates entire programs of genes involved in lipid synthesis such as cholesterol, fatty acids, triglycerides, and phospholipids. Previously, the physiological relevance of this potent activity of SREBP-1a has been thought to regulate the supply of membrane lipids in response to cell growth. Here we show that nuclear SREBP-1a and SREBP-2 bind directly to a novel SREBP binding site in the promoter of the p21WAF1/CIP1 gene, the major cyclin-dependent kinase inhibitor, and strongly activate its promoter activity. Only the SREBP-1a isoform consistently causes induction of p21 at both the mRNA and protein levels. Colony formation assays and polyploidy of livers from transgenic mice suggest that activation of p21 by SREBP-1a could inhibit cell growth. Activation of endogenous SREBPs in lipid deprivation conditions was associated with induction of p21 mRNA and protein. Expression of p21 was reduced in SREBP-1 null mice. These data suggest a physiological role of SREBP-1a in p21 regulation. Identification of p21 as a new SREBP target might implicate a new paradigm in the link between lipid synthesis and cell growth.

scholarly journals 13,16-Dimethyl Octacosanedioic Acid (iso-Diabolic Acid), a Common Membrane-Spanning Lipid of Acidobacteria Subdivisions 1 and 3

2011 ◽  
Vol 77 (12) ◽  
pp. 4147-4154 ◽  
Author(s):  
Jaap S. Sinninghe Damsté ◽  
W. Irene C. Rijpstra ◽  
Ellen C. Hopmans ◽  
Johan W. H. Weijers ◽  
Bärbel U. Foesel ◽  
...  
Keyword(s):  
Fatty Acids ◽  
High Performance ◽  
Membrane Lipids ◽  
Direct Analysis ◽  
Polar Lipids ◽  
Gas Chromatography Mass Spectrometry ◽  
Content Type ◽  
Alkyl Chains ◽  
Intact Polar Lipids ◽  
Membrane Spanning

ABSTRACTThe distribution of membrane lipids of 17 different strains representing 13 species of subdivisions 1 and 3 of the phylumAcidobacteria, a highly diverse phylum of theBacteria, were examined by hydrolysis and gas chromatography-mass spectrometry (MS) and by high-performance liquid chromatography-MS of intact polar lipids. Upon both acid and base hydrolyses of total cell material, the uncommon membrane-spanning lipid 13,16-dimethyl octacosanedioic acid (iso-diabolic acid) was released in substantial amounts (22 to 43% of the total fatty acids) from all of the acidobacteria studied. This lipid has previously been encountered only in thermophilicThermoanaerobacterspecies but bears a structural resemblance to the alkyl chains of bacterial glycerol dialkyl glycerol tetraethers (GDGTs) that occur ubiquitously in peat and soil and are suspected to be produced by acidobacteria. As reported previously, most species also containediso-C15and C16:1ω7Cas major fatty acids but the presence ofiso-diabolic acid was unnoticed in previous studies, most probably because the complex lipid that contained this moiety was not extractable from the cells; it could only be released by hydrolysis. Direct analysis of intact polar lipids in the Bligh-Dyer extract of three acidobacterial strains, indeed, did not reveal any membrane-spanning lipids containingiso-diabolic acid. In 3 of the 17 strains, ether-boundiso-diabolic acid was detected after hydrolysis of the cells, including one branched GDGT containingiso-diabolic acid-derived alkyl chains. Since the GDGT distribution in soils is much more complex, branched GDGTs in soil likely also originate from other (acido)bacteria capable of biosynthesizing these components.

scholarly journals Ether- and Ester-Boundiso-Diabolic Acid and Other Lipids in Members of Acidobacteria Subdivision 4

2014 ◽  
Vol 80 (17) ◽  
pp. 5207-5218 ◽  
Author(s):  
Jaap S. Sinninghe Damsté ◽  
W. Irene C. Rijpstra ◽  
Ellen C. Hopmans ◽  
Bärbel U. Foesel ◽  
Pia K. Wüst ◽  
...  
Keyword(s):  
High Performance ◽  
Hot Springs ◽  
Membrane Lipids ◽  
Peat Soil ◽  
Major Influence ◽  
Content Type ◽  
Fractional Abundance ◽  
Intact Polar Lipids ◽  
Membrane Spanning ◽  
Hydrolysis Of

ABSTRACTRecently,iso-diabolic acid (13,16-dimethyl octacosanedioic acid) has been identified as a major membrane-spanning lipid of subdivisions 1 and 3 of theAcidobacteria, a highly diverse phylum within theBacteria. This finding pointed to theAcidobacteriaas a potential source for the bacterial glycerol dialkyl glycerol tetraethers that occur ubiquitously in peat, soil, lakes, and hot springs. Here, we examined the lipid composition of seven phylogenetically divergent strains of subdivision 4 of theAcidobacteria, a bacterial group that is commonly encountered in soil. Acid hydrolysis of total cell material releasediso-diabolic acid derivatives in substantial quantities (11 to 48% of all fatty acids). In contrast to subdivisions 1 and 3 of theAcidobacteria, 6 out of the 7 species of subdivision 4 (excepting “CandidatusChloracidobacterium thermophilum”) containediso-diabolic acid ether bound to a glycerol in larger fractional abundance thaniso-diabolic acid itself. This is in agreement with the analysis of intact polar lipids (IPLs) by high-performance liquid chromatography-mass spectrometry (HPLC-MS), which showed the dominance of mixed ether-ester glycerides.iso-Diabolic acid-containing IPLs were not identified, because these IPLs are not released with a Bligh-Dyer extraction, as observed before when studying lipid compositions of subdivisions 1 and 3 of theAcidobacteria. The presence of ether bonds in the membrane lipids does not seem to be an adaptation to temperature, because the five mesophilic isolates contained a larger amount of ether lipids than the thermophile “Ca. Chloracidobacterium thermophilum.” Furthermore, experiments withPyrinomonas methylaliphatogenesdid not reveal a major influence of growth temperature over the 50 to 69°C range.

Membrane lipid profile monitored by mass spectrometry detected differences between fresh and vitrified in vitro-produced bovine embryos

Zygote ◽  
2014 ◽  
Vol 23 (5) ◽  
pp. 732-741 ◽  
Author(s):  
Beatriz C. S. Leão ◽  
Nathália A. S. Rocha-Frigoni ◽  
Elaine C. Cabral ◽  
Marcos F. Franco ◽  
Christina R. Ferreira ◽  
...  
Keyword(s):  
Mass Spectrometry ◽  
Lipid Profile ◽  
Membrane Lipids ◽  
Membrane Lipid ◽  
Maldi Ms ◽  
Charge Ratio ◽  
Alkyl Ether ◽  
Bovine Embryos ◽  
The Impact

SummaryThis study aimed to evaluate the impact of vitrification on membrane lipid profile obtained by mass spectrometry (MS) of in vitro-produced bovine embryos. Matrix-assisted laser desorption ionization–mass spectrometry (MALDI–MS) has been used to obtain individual embryo membrane lipid profiles. Due to conditions of analysis, mainly membrane lipids, most favorably phosphatidylcholines (PCs) and sphingomyelins (SMs) have been detected. The following ions described by their mass-to-charge ratio (m/z) and respective attribution presented increased relative abundance (1.2–20×) in the vitrified group: 703.5 [SM (16:0) + H]+; 722.5 [PC (40:3) + Na]+; 758.5 [PC (34:2) + H]+; 762.5 [PC (34:0) + H]+; 790.5 [PC (36:0) + H]+ and 810.5 [PC (38:4) + H]+ and/or [PC (36:1) + Na]+. The ion with a m/z 744.5 [PCp (34:1) and/or PCe (34:2)] was 3.4-fold more abundant in the fresh group. Interestingly, ions with m/z 722.5 or 744.5 indicate the presence of lipid species, which are more resistant to enzymatic degradation as they contain fatty acyl residues linked through ether type bonds (alkyl ether or plasmalogens, indicated by the lowercase ‘e’ and ‘p‘, respectively) to the glycerol structure. The results indicate that cryopreservation impacts the membrane lipid profile, and that these alterations can be properly monitored by MALDI-MS. Membrane lipids can therefore be evaluated by MALDI-MS to monitor the effect of cryopreservation on membrane lipids, and to investigate changes in lipid profile that may reflect the metabolic response to the cryopreservation stress or changes in the environmental conditions.

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