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

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 adap...

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Autores principales:	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
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2021
Materias:	Thioalkalivibrio soda lake system biology RNA-Seq membrane lipid composition glycine betaine Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/b41ac1994cf8410b85ea387a2b0c102d
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spelling	oai:doaj.org-article:b41ac1994cf8410b85ea387a2b0c102d2021-12-02T18:21:20ZMolecular and Physiological Adaptations to Low Temperature in <italic toggle="yes">Thioalkalivibrio</italic> Strains Isolated from Soda Lakes with Different Temperature Regimes10.1128/mSystems.01202-202379-5077https://doaj.org/article/b41ac1994cf8410b85ea387a2b0c102d2021-04-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.01202-20https://doaj.org/toc/2379-5077ABSTRACT 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. Author Video: An author video summary of this article is available.Anne-Catherine AhnEvelien JongepierJ. Merijn SchuurmansW. Irene C. RijpstraJaap S. Sinninghe DamstéErwin A. GalinskiPawel RomanDimitry SorokinGerard MuyzerAmerican Society for MicrobiologyarticleThioalkalivibriosoda lakesystem biologyRNA-Seqmembrane lipid compositionglycine betaineMicrobiologyQR1-502ENmSystems, Vol 6, Iss 2 (2021)
institution	DOAJ
collection	DOAJ
language	EN
topic	Thioalkalivibrio soda lake system biology RNA-Seq membrane lipid composition glycine betaine Microbiology QR1-502
spellingShingle	Thioalkalivibrio soda lake system biology RNA-Seq membrane lipid composition glycine betaine Microbiology QR1-502 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 Molecular and Physiological Adaptations to Low Temperature in <italic toggle="yes">Thioalkalivibrio</italic> Strains Isolated from Soda Lakes with Different Temperature Regimes
description	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. Author Video: An author video summary of this article is available.
format	article
author	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
author_facet	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
author_sort	Anne-Catherine Ahn
title	Molecular and Physiological Adaptations to Low Temperature in <italic toggle="yes">Thioalkalivibrio</italic> Strains Isolated from Soda Lakes with Different Temperature Regimes
title_short	Molecular and Physiological Adaptations to Low Temperature in <italic toggle="yes">Thioalkalivibrio</italic> Strains Isolated from Soda Lakes with Different Temperature Regimes
title_full	Molecular and Physiological Adaptations to Low Temperature in <italic toggle="yes">Thioalkalivibrio</italic> Strains Isolated from Soda Lakes with Different Temperature Regimes
title_fullStr	Molecular and Physiological Adaptations to Low Temperature in <italic toggle="yes">Thioalkalivibrio</italic> Strains Isolated from Soda Lakes with Different Temperature Regimes
title_full_unstemmed	Molecular and Physiological Adaptations to Low Temperature in <italic toggle="yes">Thioalkalivibrio</italic> Strains Isolated from Soda Lakes with Different Temperature Regimes
title_sort	molecular and physiological adaptations to low temperature in <italic toggle="yes">thioalkalivibrio</italic> strains isolated from soda lakes with different temperature regimes
publisher	American Society for Microbiology
publishDate	2021
url	https://doaj.org/article/b41ac1994cf8410b85ea387a2b0c102d
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Molecular and Physiological Adaptations to Low Temperature in <italic toggle="yes">Thioalkalivibrio</italic> Strains Isolated from Soda Lakes with Different Temperature Regimes

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