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Adaptation to Varying Salinity in Halomonas elongata: Much More Than Ectoine Accumulation

The halophilic γ-proteobacterium Halomonas elongata DSM 2581(T) thrives at salt concentrations well above 10 % NaCl (1.7 M NaCl). A well-known osmoregulatory mechanism is the accumulation of the compatible solute ectoine within the cell in response to osmotic stress. While ectoine accumulation is ce...

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Autores principales: Hobmeier, Karina, Cantone, Martina, Nguyen, Quynh Anh, Pflüger-Grau, Katharina, Kremling, Andreas, Kunte, Hans Jörg, Pfeiffer, Friedhelm, Marin-Sanguino, Alberto
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9006882/
https://www.ncbi.nlm.nih.gov/pubmed/35432243
http://dx.doi.org/10.3389/fmicb.2022.846677
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author Hobmeier, Karina
Cantone, Martina
Nguyen, Quynh Anh
Pflüger-Grau, Katharina
Kremling, Andreas
Kunte, Hans Jörg
Pfeiffer, Friedhelm
Marin-Sanguino, Alberto
author_facet Hobmeier, Karina
Cantone, Martina
Nguyen, Quynh Anh
Pflüger-Grau, Katharina
Kremling, Andreas
Kunte, Hans Jörg
Pfeiffer, Friedhelm
Marin-Sanguino, Alberto
author_sort Hobmeier, Karina
collection PubMed
description The halophilic γ-proteobacterium Halomonas elongata DSM 2581(T) thrives at salt concentrations well above 10 % NaCl (1.7 M NaCl). A well-known osmoregulatory mechanism is the accumulation of the compatible solute ectoine within the cell in response to osmotic stress. While ectoine accumulation is central to osmoregulation and promotes resistance to high salinity in halophilic bacteria, ectoine has this effect only to a much lesser extent in non-halophiles. We carried out transcriptome analysis of H. elongata grown on two different carbon sources (acetate or glucose), and low (0.17 M NaCl), medium (1 M), and high salinity (2 M) to identify additional mechanisms for adaptation to high saline environments. To avoid a methodological bias, the transcripts were evaluated by applying two methods, DESeq2 and Transcripts Per Million (TPM). The differentially transcribed genes in response to the available carbon sources and salt stress were then compared to the transcriptome profile of Chromohalobacter salexigens, a closely related moderate halophilic bacterium. Transcriptome profiling supports the notion that glucose is degraded via the cytoplasmic Entner-Doudoroff pathway, whereas the Embden-Meyerhoff-Parnas pathway is employed for gluconeogenesis. The machinery of oxidative phosphorylation in H. elongata and C. salexigens differs greatly from that of non-halophilic organisms, and electron flow can occur from quinone to oxygen along four alternative routes. Two of these pathways via cytochrome bo' and cytochrome bd quinol oxidases seem to be upregulated in salt stressed cells. Among the most highly regulated genes in H. elongata and C. salexigens are those encoding chemotaxis and motility proteins, with genes for chemotaxis and flagellar assembly severely downregulated at low salt concentrations. We also compared transcripts at low and high-salt stress (low growth rate) with transcripts at optimal salt concentration and found that the majority of regulated genes were down-regulated in stressed cells, including many genes involved in carbohydrate metabolism, while ribosome synthesis was up-regulated, which is in contrast to what is known from non-halophiles at slow growth. Finally, comparing the acidity of the cytoplasmic proteomes of non-halophiles, extreme halophiles and moderate halophiles suggests adaptation to an increased cytoplasmic ion concentration of H. elongata. Taken together, these results lead us to propose a model for salt tolerance in H. elongata where ion accumulation plays a greater role in salt tolerance than previously assumed.
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spelling pubmed-90068822022-04-14 Adaptation to Varying Salinity in Halomonas elongata: Much More Than Ectoine Accumulation Hobmeier, Karina Cantone, Martina Nguyen, Quynh Anh Pflüger-Grau, Katharina Kremling, Andreas Kunte, Hans Jörg Pfeiffer, Friedhelm Marin-Sanguino, Alberto Front Microbiol Microbiology The halophilic γ-proteobacterium Halomonas elongata DSM 2581(T) thrives at salt concentrations well above 10 % NaCl (1.7 M NaCl). A well-known osmoregulatory mechanism is the accumulation of the compatible solute ectoine within the cell in response to osmotic stress. While ectoine accumulation is central to osmoregulation and promotes resistance to high salinity in halophilic bacteria, ectoine has this effect only to a much lesser extent in non-halophiles. We carried out transcriptome analysis of H. elongata grown on two different carbon sources (acetate or glucose), and low (0.17 M NaCl), medium (1 M), and high salinity (2 M) to identify additional mechanisms for adaptation to high saline environments. To avoid a methodological bias, the transcripts were evaluated by applying two methods, DESeq2 and Transcripts Per Million (TPM). The differentially transcribed genes in response to the available carbon sources and salt stress were then compared to the transcriptome profile of Chromohalobacter salexigens, a closely related moderate halophilic bacterium. Transcriptome profiling supports the notion that glucose is degraded via the cytoplasmic Entner-Doudoroff pathway, whereas the Embden-Meyerhoff-Parnas pathway is employed for gluconeogenesis. The machinery of oxidative phosphorylation in H. elongata and C. salexigens differs greatly from that of non-halophilic organisms, and electron flow can occur from quinone to oxygen along four alternative routes. Two of these pathways via cytochrome bo' and cytochrome bd quinol oxidases seem to be upregulated in salt stressed cells. Among the most highly regulated genes in H. elongata and C. salexigens are those encoding chemotaxis and motility proteins, with genes for chemotaxis and flagellar assembly severely downregulated at low salt concentrations. We also compared transcripts at low and high-salt stress (low growth rate) with transcripts at optimal salt concentration and found that the majority of regulated genes were down-regulated in stressed cells, including many genes involved in carbohydrate metabolism, while ribosome synthesis was up-regulated, which is in contrast to what is known from non-halophiles at slow growth. Finally, comparing the acidity of the cytoplasmic proteomes of non-halophiles, extreme halophiles and moderate halophiles suggests adaptation to an increased cytoplasmic ion concentration of H. elongata. Taken together, these results lead us to propose a model for salt tolerance in H. elongata where ion accumulation plays a greater role in salt tolerance than previously assumed. Frontiers Media S.A. 2022-03-30 /pmc/articles/PMC9006882/ /pubmed/35432243 http://dx.doi.org/10.3389/fmicb.2022.846677 Text en Copyright © 2022 Hobmeier, Cantone, Nguyen, Pflüger-Grau, Kremling, Kunte, Pfeiffer and Marin-Sanguino. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Microbiology
Hobmeier, Karina
Cantone, Martina
Nguyen, Quynh Anh
Pflüger-Grau, Katharina
Kremling, Andreas
Kunte, Hans Jörg
Pfeiffer, Friedhelm
Marin-Sanguino, Alberto
Adaptation to Varying Salinity in Halomonas elongata: Much More Than Ectoine Accumulation
title Adaptation to Varying Salinity in Halomonas elongata: Much More Than Ectoine Accumulation
title_full Adaptation to Varying Salinity in Halomonas elongata: Much More Than Ectoine Accumulation
title_fullStr Adaptation to Varying Salinity in Halomonas elongata: Much More Than Ectoine Accumulation
title_full_unstemmed Adaptation to Varying Salinity in Halomonas elongata: Much More Than Ectoine Accumulation
title_short Adaptation to Varying Salinity in Halomonas elongata: Much More Than Ectoine Accumulation
title_sort adaptation to varying salinity in halomonas elongata: much more than ectoine accumulation
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9006882/
https://www.ncbi.nlm.nih.gov/pubmed/35432243
http://dx.doi.org/10.3389/fmicb.2022.846677
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