Abstract
ABSTRACTThe 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.Author Video: An author video summary of this article is available.
Highlights
Soda lakes are extreme haloalkaline environments with a high microbial diversity despite their harsh conditions [1,2,3]
We studied the molecular and physiological adaptation mechanisms of two moderate halophilic Thioalkalivibrio strains, Thioalkalivibrio versutus AL2T and Thioalkalivibrio nitratis ALJ2, to low temperature. These strains were chosen because they were isolated from soda lakes with different temperature regimes: T. versutus AL2T was isolated from Lake Hadyn in southeastern Siberia, where it is subjected to strong seasonal fluctuations with freezing temperatures in winter and warm summers [17, 34], while T. nitratis ALJ2 originates from Lake Elmenteita in the East African Rift Valley with a constant temperature of ca. 20°C the year round [7, 17]
Batch cultivation showed that T. versutus AL2T grew much faster than T. nitratis ALJ2 at 10°C, while this was the opposite at 30°C (Table 1)
Summary
Soda lakes are extreme haloalkaline environments with a high microbial diversity despite their harsh conditions [1,2,3]. Certain lakes are exposed to fluctuating temperatures throughout the year, whereas others are located in regions with a stable temperature profile Despite these multiple extreme conditions, various bacteria and archaea and some eukaryotes can thrive in these lakes [1, 5, 9,10,11]. Negative supercoiling of DNA [23] and overstabilization of secondary structures in RNA [24, 25] are corrected by helicases [26] and cold shock proteins [27, 28] and protein misfolding [29] by chaperones such as GroEL and GroES [30] Another stressor that accompanies the drop in temperature is the increased formation of reactive oxygen species (ROS) [31] due to higher solubility of oxygen at low temperatures [32]. 2.92 6 0.087 3.41 6 0.081 to low temperature, we studied gene expression by transcriptomics, including strain-specific responses to temperature, and analyzed their adaptation of membrane lipid composition and the production of the cryoprotectant glycine betaine at both 10°C and 30°C
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