Molecular and Physiological Adaptations to Low Temperature in <italic toggle='yes'>Thioalkalivibrio</italic> Strains Isolated from Soda Lakes with Different Temperature Regimes

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 Citation Ahn A-C, Jongepier E, Schuurmans JM, Rijpstra WIC, Sinninghe Damsté JS, Galinski EA, Roman P, Sorokin D, Muyzer G. 2021. Molecular and physiological adaptations to low temperature in Thioalkalivibrio strains isolated from soda lakes with different temperature regimes. mSystems 6:e01202-20. https://doi.org/10.1128/mSystems.01202-20. Editor Rachel Mackelprang, California State University, Northridge Copyright © 2021 Ahn et al. This is an openaccess article distributed under the terms of the Creative Commons Attribution 4.0 International license. Address correspondence to Gerard Muyzer, g.muijzer@uva.nl. Low-temperature adaptation in Thioalkalivibrio Received 16 November 2020 Accepted 30 March 2021 Published 27 April 2021 March/April 2021 Volume 6 Issue 2 e01202-20 msystems.asm. org 1 RESEARCH ARTICLE