Cargando…

Transcriptomic analysis of chloride tolerance in Leptospirillum ferriphilum DSM 14647 adapted to NaCl

Chloride ions are toxic for most acidophilic microorganisms. In this study, the chloride tolerance mechanisms in the acidophilic iron-oxidizing bacterium Leptospirillum ferriphilum DSM 14647 adapted to 180 mM NaCl were investigated by a transcriptomic approach. Results showed that 99 genes were diff...

Descripción completa

Detalles Bibliográficos
Autores principales: Rivera-Araya, Javier, Heine, Thomas, Chávez, Renato, Schlömann, Michael, Levicán, Gloria
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9053815/
https://www.ncbi.nlm.nih.gov/pubmed/35486621
http://dx.doi.org/10.1371/journal.pone.0267316
_version_ 1784697054349492224
author Rivera-Araya, Javier
Heine, Thomas
Chávez, Renato
Schlömann, Michael
Levicán, Gloria
author_facet Rivera-Araya, Javier
Heine, Thomas
Chávez, Renato
Schlömann, Michael
Levicán, Gloria
author_sort Rivera-Araya, Javier
collection PubMed
description Chloride ions are toxic for most acidophilic microorganisms. In this study, the chloride tolerance mechanisms in the acidophilic iron-oxidizing bacterium Leptospirillum ferriphilum DSM 14647 adapted to 180 mM NaCl were investigated by a transcriptomic approach. Results showed that 99 genes were differentially expressed in the adapted versus the non-adapted cultures, of which 69 and 30 were significantly up-regulated or down-regulated, respectively. Genes that were up-regulated include carbonic anhydrase, cytochrome c oxidase (ccoN) and sulfide:quinone reductase (sqr), likely involved in intracellular pH regulation. Towards the same end, the cation/proton antiporter CzcA (czcA) was down-regulated. Adapted cells showed a higher oxygen consumption rate (2.2 x 10(−9) ppm O(2) s(-1)cell(-1)) than non-adapted cells (1.2 x 10(−9) ppm O(2) s(-1)cell(-1)). Genes coding for the antioxidants flavohemoprotein and cytochrome c peroxidase were also up-regulated. Measurements of the intracellular reactive oxygen species (ROS) level revealed that adapted cells had a lower level than non-adapted cells, suggesting that detoxification of ROS could be an important strategy to withstand NaCl. In addition, data analysis revealed the up-regulation of genes for Fe-S cluster biosynthesis (iscR), metal reduction (merA) and activation of a cellular response mediated by diffusible signal factors (DSFs) and the second messenger c-di-GMP. Several genes related to the synthesis of lipopolysaccharide and peptidoglycan were consistently down-regulated. Unexpectedly, the genes ectB, ectC and ectD involved in the biosynthesis of the compatible solutes (hydroxy)ectoine were also down-regulated. In line with these findings, although hydroxyectoine reached 20 nmol mg(-1) of wet biomass in non-adapted cells, it was not detected in L. ferriphilum adapted to NaCl, suggesting that this canonical osmotic stress response was dispensable for salt adaptation. Differentially expressed transcripts and experimental validations suggest that adaptation to chloride in acidophilic microorganisms involves a multifactorial response that is different from the response in other bacteria studied.
format Online
Article
Text
id pubmed-9053815
institution National Center for Biotechnology Information
language English
publishDate 2022
publisher Public Library of Science
record_format MEDLINE/PubMed
spelling pubmed-90538152022-04-30 Transcriptomic analysis of chloride tolerance in Leptospirillum ferriphilum DSM 14647 adapted to NaCl Rivera-Araya, Javier Heine, Thomas Chávez, Renato Schlömann, Michael Levicán, Gloria PLoS One Research Article Chloride ions are toxic for most acidophilic microorganisms. In this study, the chloride tolerance mechanisms in the acidophilic iron-oxidizing bacterium Leptospirillum ferriphilum DSM 14647 adapted to 180 mM NaCl were investigated by a transcriptomic approach. Results showed that 99 genes were differentially expressed in the adapted versus the non-adapted cultures, of which 69 and 30 were significantly up-regulated or down-regulated, respectively. Genes that were up-regulated include carbonic anhydrase, cytochrome c oxidase (ccoN) and sulfide:quinone reductase (sqr), likely involved in intracellular pH regulation. Towards the same end, the cation/proton antiporter CzcA (czcA) was down-regulated. Adapted cells showed a higher oxygen consumption rate (2.2 x 10(−9) ppm O(2) s(-1)cell(-1)) than non-adapted cells (1.2 x 10(−9) ppm O(2) s(-1)cell(-1)). Genes coding for the antioxidants flavohemoprotein and cytochrome c peroxidase were also up-regulated. Measurements of the intracellular reactive oxygen species (ROS) level revealed that adapted cells had a lower level than non-adapted cells, suggesting that detoxification of ROS could be an important strategy to withstand NaCl. In addition, data analysis revealed the up-regulation of genes for Fe-S cluster biosynthesis (iscR), metal reduction (merA) and activation of a cellular response mediated by diffusible signal factors (DSFs) and the second messenger c-di-GMP. Several genes related to the synthesis of lipopolysaccharide and peptidoglycan were consistently down-regulated. Unexpectedly, the genes ectB, ectC and ectD involved in the biosynthesis of the compatible solutes (hydroxy)ectoine were also down-regulated. In line with these findings, although hydroxyectoine reached 20 nmol mg(-1) of wet biomass in non-adapted cells, it was not detected in L. ferriphilum adapted to NaCl, suggesting that this canonical osmotic stress response was dispensable for salt adaptation. Differentially expressed transcripts and experimental validations suggest that adaptation to chloride in acidophilic microorganisms involves a multifactorial response that is different from the response in other bacteria studied. Public Library of Science 2022-04-29 /pmc/articles/PMC9053815/ /pubmed/35486621 http://dx.doi.org/10.1371/journal.pone.0267316 Text en © 2022 Rivera-Araya et al https://creativecommons.org/licenses/by/4.0/This is an open access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Rivera-Araya, Javier
Heine, Thomas
Chávez, Renato
Schlömann, Michael
Levicán, Gloria
Transcriptomic analysis of chloride tolerance in Leptospirillum ferriphilum DSM 14647 adapted to NaCl
title Transcriptomic analysis of chloride tolerance in Leptospirillum ferriphilum DSM 14647 adapted to NaCl
title_full Transcriptomic analysis of chloride tolerance in Leptospirillum ferriphilum DSM 14647 adapted to NaCl
title_fullStr Transcriptomic analysis of chloride tolerance in Leptospirillum ferriphilum DSM 14647 adapted to NaCl
title_full_unstemmed Transcriptomic analysis of chloride tolerance in Leptospirillum ferriphilum DSM 14647 adapted to NaCl
title_short Transcriptomic analysis of chloride tolerance in Leptospirillum ferriphilum DSM 14647 adapted to NaCl
title_sort transcriptomic analysis of chloride tolerance in leptospirillum ferriphilum dsm 14647 adapted to nacl
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9053815/
https://www.ncbi.nlm.nih.gov/pubmed/35486621
http://dx.doi.org/10.1371/journal.pone.0267316
work_keys_str_mv AT riveraarayajavier transcriptomicanalysisofchloridetoleranceinleptospirillumferriphilumdsm14647adaptedtonacl
AT heinethomas transcriptomicanalysisofchloridetoleranceinleptospirillumferriphilumdsm14647adaptedtonacl
AT chavezrenato transcriptomicanalysisofchloridetoleranceinleptospirillumferriphilumdsm14647adaptedtonacl
AT schlomannmichael transcriptomicanalysisofchloridetoleranceinleptospirillumferriphilumdsm14647adaptedtonacl
AT levicangloria transcriptomicanalysisofchloridetoleranceinleptospirillumferriphilumdsm14647adaptedtonacl