scholarly journals Molecular and Physiological Adaptations to Low Temperature in Thioalkalivibrio Strains Isolated from Soda Lakes with Different Temperature Regimes

mSystems ◽  
2021 ◽  
Vol 6 (2) ◽  
Author(s):  
Anne-Catherine Ahn ◽  
Evelien Jongepier ◽  
J. Merijn Schuurmans ◽  
W. Irene C. Rijpstra ◽  
Jaap S. Sinninghe Damsté ◽  
...  

ABSTRACT The genus Thioalkalivibrio comprises sulfur-oxidizing bacteria thriving in soda lakes at high pH and salinity. Depending on the geographical location and the season, these lakes can strongly vary in temperature. To obtain a comprehensive understanding of the molecular and physiological adaptations to low temperature, we compared the responses of two Thioalkalivibrio strains to low (10°C) and high (30°C) temperatures. For this, the strains were grown under controlled conditions in chemostats and analyzed for their gene expression (RNA sequencing [RNA-Seq]), membrane lipid composition, and glycine betaine content. The strain Thioalkalivibrio versutus AL2T originated from a soda lake in southeast Siberia that is exposed to strong seasonal temperature differences, including freezing winters, whereas Thioalkalivibrio nitratis ALJ2 was isolated from an East African Rift Valley soda lake with a constant warm temperature the year round. The strain AL2T grew faster than ALJ2 at 10°C, likely due to its 3-fold-higher concentration of the osmolyte glycine betaine. Moreover, significant changes in the membrane lipid composition were observed for both strains, leading to an increase in their unsaturated fatty acid content via the Fab pathway to avoid membrane stiffness. Genes for the transcriptional and translational machinery, as well as for counteracting cold-induced hampering of nucleotides and proteins, were upregulated. Oxidative stress was reduced by induction of vitamin B12 biosynthesis genes, and growth at 10°C provoked downregulation of genes involved in the second half of the sulfur oxidation pathway. Genes for intracellular signal transduction were differentially expressed, and interestingly, AL2T upregulated flagellin expression, whereas ALJ2 downregulated it. IMPORTANCE In addition to their haloalkaline conditions, soda lakes can also harbor a variety of other extreme parameters, to which their microbial communities need to adapt. However, for most of these supplementary stressors, it is not well known yet how haloalkaliphiles adapt and resist. Here, we studied the strategy for adaptation to low temperature in the haloalkaliphilic genus Thioalkalivibrio by using two strains isolated from soda lakes with different temperature regimes. Even though the strains showed a strong difference in growth rate at 10°C, they exhibited similar molecular and physiological adaptation responses. We hypothesize that they take advantage of resistance mechanisms against other stressors commonly found in soda lakes, which are therefore maintained in the bacteria living in the absence of low-temperature pressure. A major difference, however, was detected for their glycine betaine content at 10°C, highlighting the power of this osmolyte to also act as a key compound in cryoprotection.

2017 ◽  
Vol 83 (18) ◽  
Author(s):  
Yanli Qi ◽  
Hui Liu ◽  
Jiayin Yu ◽  
Xiulai Chen ◽  
Liming Liu

ABSTRACT Candida glabrata is a promising producer of organic acids. To elucidate the physiological function of the Mediator tail subunit Med15B in the response to low-pH stress, we constructed a deletion strain, C. glabrata med15BΔ, and an overexpression strain, C. glabrata HTUΔ/CgMED15B. Deletion of MED15B caused biomass production, glucose consumption rate, and cell viability to decrease by 28.3%, 31.7%, and 26.5%, respectively, compared with those of the parent (HTUΔ) strain at pH 2.0. Expression of lipid metabolism-related genes was significantly downregulated in the med15BΔ strain, whereas key genes of ergosterol biosynthesis showed abnormal upregulation. This caused the proportion of C18:1 fatty acids, the ratio of unsaturated to saturated fatty acids (UFA/SFA), and the total phospholipid content to decrease by 11.6%, 27.4%, and 37.6%, respectively. Cells failed to synthesize fecosterol and ergosterol, leading to the accumulation and a 60.3-fold increase in the concentration of zymosterol. Additionally, cells showed reductions of 69.2%, 11.6%, and 21.8% in membrane integrity, fluidity, and H+-ATPase activity, respectively. In contrast, overexpression of Med15B increased the C18:1 levels, total phospholipids, ergosterol content, and UFA/SFA by 18.6%, 143.5%, 94.5%, and 18.7%, respectively. Membrane integrity, fluidity, and H+-ATPase activity also increased by 30.2%, 6.9%, and 51.8%, respectively. Furthermore, in the absence of pH buffering, dry weight of cells and pyruvate concentrations were 29.3% and 61.2% higher, respectively, than those of the parent strain. These results indicated that in C. glabrata, Med15B regulates tolerance toward low pH via transcriptional regulation of acid stress response genes and alteration in lipid composition. IMPORTANCE This study explored the role of the Mediator tail subunit Med15B in the metabolism of Candida glabrata under acidic conditions. Overexpression of MED15B enhanced yeast tolerance to low pH and improved biomass production, cell viability, and pyruvate yield. Membrane lipid composition data indicated that Med15B might play a critical role in membrane integrity, fluidity, and H+-ATPase activity homeostasis at low pH. Thus, controlling membrane composition may serve to increase C. glabrata productivity at low pH.


1988 ◽  
Vol 254 (6) ◽  
pp. R870-R876 ◽  
Author(s):  
N. L. Pruitt

The membrane lipid composition of hepatopancreas tissue was analyzed from two phylogenetically related species of crayfish after thermal acclimation to either 5 or 20 degrees C. One species overwinters in a quiescent state (Orconectes propinquus) and the other remains active throughout the winter (Cambarus bartoni). Both species significantly decreased the level of saturates in the major phosphatides, phosphatidylcholine (PC) and phosphatidylethanolamine (PE; difference not significant in C. bartoni), and both winter-active and winter-quiescent animals tended to be enriched in n-3 acids in PC. Orconectes animals tended to be enriched in n - 3 acids in PC. Orconectes accumulated n - 6 acids in PE at low temperature, whereas Cambarus lost n - 6 acids in this lipid, a change that was offset by the accumulation of monoenes. Cardiolipin became more saturated with cold acclimation in both species. The fatty acid content of the triacylglycerol fraction showed little change with acclimation history, although O. propinquus did accumulate n - 3 acids in triglycerides at low temperature. In O. propinquus, head-group composition was not significantly altered by temperature, but in C. bartoni, cold temperature increased the relative amounts of PE, sphingomyelin, and phosphatidylinositol at the expense of PC. Adaptations to temperature in membrane composition of poikilotherms are related to the overwintering strategy of the animal.


2016 ◽  
Vol 82 (23) ◽  
pp. 6920-6929 ◽  
Author(s):  
Dongni Yan ◽  
Xiaobao Lin ◽  
Yanli Qi ◽  
Hui Liu ◽  
Xiulai Chen ◽  
...  

ABSTRACTThe asexual facultative aerobic haploid yeastCandida glabratais widely used in the industrial production of various organic acids. To elucidate the physiological function of theC. glabratatranscription factor Crz1p (CgCrz1p) and its role in tolerance to acid stress, we deleted or overexpressed the corresponding gene,CgCRZ1. Deletion ofCgCRZ1resulted in a 60% decrease in the dry weight of cells (DCW) and a 50% drop in cell viability compared with those of the wild type at pH 2.0. Expression of lipid metabolism-associated genes was also significantly downregulated. Consequently, the proportion of C18:1fatty acids, the ratio of unsaturated to saturated fatty acids, and the ergosterol content decreased by 30%, 46%, and 30%, respectively. Additionally, membrane integrity, fluidity, and H+-ATPase activity were reduced by 45%, 9%, and 50%, respectively. In contrast, overexpression of CgCrz1p increased C18:1and ergosterol contents by 16% and 40%, respectively. Overexpression also enhanced membrane integrity, fluidity, and H+-ATPase activity by 31%, 6%, and 20%, respectively. Moreover, in the absence of pH buffering, the DCW and pyruvate titers increased by 48% and 60%, respectively, compared to that of the wild type. Together, these results suggest that CgCrz1p regulates tolerance to acidic conditions by altering membrane lipid composition inC. glabrata.IMPORTANCEThis study provides insight into the metabolism ofCandida glabrataunder acidic conditions, such as those encountered during the industrial production of organic acids. We found that overexpression of the transcription factor CgCrz1p improved viability, biomass, and pyruvate yields at a low pH. Analysis of plasma membrane lipid composition indicated that CgCrz1p might play an important role in its integrity and fluidity and that it enhanced the pumping of protons in acidic environments. We propose that altering the structure of the cell membrane may provide a successful strategy for increasingC. glabrataproductivity at a low pH.


2016 ◽  
Vol 82 (15) ◽  
pp. 4505-4516 ◽  
Author(s):  
Kevin W. Becker ◽  
Felix J. Elling ◽  
Marcos Y. Yoshinaga ◽  
Andrea Söllinger ◽  
Tim Urich ◽  
...  

ABSTRACTA new clade of archaea has recently been proposed to constitute the seventh methanogenic order, theMethanomassiliicoccales, which is related to theThermoplasmatalesand the uncultivated archaeal clades deep-sea hydrothermal ventEuryarchaeotagroup 2 and marine group IIEuryarchaeotabut only distantly related to other methanogens. In this study, we investigated the membrane lipid composition ofMethanomassiliicoccus luminyensis, the sole cultured representative of this seventh order. The lipid inventory ofM. luminyensiscomprises a unique assemblage of novel lipids as well as lipids otherwise typical for thermophilic, methanogenic, or halophilic archaea. For instance, glycerol sesterpanyl-phytanyl diether core lipids found mainly in halophilic archaea were detected, and so were compounds bearing either heptose or methoxylated glycosidic head groups, neither of which have been reported so far for other archaea. The absence of quinones or methanophenazines is consistent with a biochemistry of methanogenesis different from that of the methanophenazine-containing methylotrophic methanogens. The most distinctive characteristic of the membrane lipid composition ofM. luminyensis, however, is the presence of tetraether lipids in which one glycerol backbone is replaced by either butane- or pentanetriol, i.e., lipids recently discovered in marine sediments. Butanetriol dibiphytanyl glycerol tetraether (BDGT) constitutes the most abundant core lipid type (>50% relative abundance) inM. luminyensis. We have thus identified a source for these unusual orphan lipids. The complementary analysis of diverse marine sediment samples showed that BDGTs are widespread in anoxic layers, suggesting an environmental significance ofMethanomassiliicoccalesand/or related BDGT producers beyond gastrointestinal tracts.IMPORTANCECellular membranes of members of all three domains of life,Archaea,Bacteria, andEukarya, are largely formed by lipids in which glycerol serves as backbone for the hydrophobic alkyl chains. Recently, however, archaeal tetraether lipids with either butanetriol or pentanetriol as a backbone were identified in marine sediments and attributed to uncultured sediment-dwelling archaea. Here we show that the butanetriol-based dibiphytanyl tetraethers constitute the major lipids inMethanomassiliicoccus luminyensis, currently the only isolate of the novel seventh order of methanogens. Given the absence of these lipids in a large set of archaeal isolates, these compounds may be diagnostic for theMethanomassiliicoccalesand/or closely related archaea.


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