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

Anne-Catherine Ahn; Evelien Jongepier; J Merijn Schuurmans; W Irene C Rijpstra; Jaap S Sinninghe Damsté; Erwin A Galinski; Pawel Roman; Dimitry Sorokin; Gerard Muyzer

doi:10.1128/mSystems.01202-20

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

mSystems. 2021 Apr 27;6(2):e01202-20. doi: 10.1128/mSystems.01202-20.

Authors

Affiliations

¹ Microbial Systems Ecology, Department of Freshwater and Marine Ecology, Institute for Biodiversity and Ecosystem Dynamics, University of Amsterdam, Amsterdam, The Netherlands.
² Department of Marine Microbiology and Biogeochemistry, NIOZ Royal Netherlands Institute for Sea Research and Utrecht University, Den Burg, The Netherlands.
³ Department of Earth Sciences, Faculty of Geosciences, Utrecht University, Utrecht, The Netherlands.
⁴ Institute of Microbiology and Biotechnology, Rheinische Friedrich-Wilhelms University, Bonn, Germany.
⁵ Wetsus, European Centre of Excellence for Sustainable Water Technology, Leeuwarden, The Netherlands.
⁶ Winogradsky Institute of Microbiology, Research Centre of Biotechnology, Russian Academy of Sciences, Moscow, Russia.
⁷ Department of Biotechnology, Delft University of Technology, Delft, The Netherlands.
⁸ Microbial Systems Ecology, Department of Freshwater and Marine Ecology, Institute for Biodiversity and Ecosystem Dynamics, University of Amsterdam, Amsterdam, The Netherlands g.muijzer@uva.nl.

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 AL2^T 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 AL2^T 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, AL2^T 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.

Keywords: RNA-Seq; Thioalkalivibrio; glycine betaine; membrane lipid composition; soda lake; system biology.