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...
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| Vydané v: | PloS one Ročník 17; číslo 4; s. e0267316 |
|---|---|
| Hlavní autori: | , , , , |
| Médium: | Journal Article |
| Jazyk: | English |
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United States
Public Library of Science
29.04.2022
Public Library of Science (PLoS) |
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| ISSN: | 1932-6203, 1932-6203 |
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| Abstract | 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. |
|---|---|
| AbstractList | 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 O2 s-1cell-1) than non-adapted cells (1.2 x 10−9 ppm O2 s-1cell-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. 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.sup.-9 ppm O.sub.2 s.sup.-1 cell.sup.-1) than non-adapted cells (1.2 x 10.sup.-9 ppm O.sub.2 s.sup.-1 cell.sup.-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.sup.-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. 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 O2 s-1cell-1) than non-adapted cells (1.2 x 10-9 ppm O2 s-1cell-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. 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 O2 s-1cell-1) than non-adapted cells (1.2 x 10-9 ppm O2 s-1cell-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.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 O2 s-1cell-1) than non-adapted cells (1.2 x 10-9 ppm O2 s-1cell-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. 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. |
| Audience | Academic |
| Author | Heine, Thomas Chávez, Renato Schlömann, Michael Levicán, Gloria Rivera-Araya, Javier |
| AuthorAffiliation | 1 Biology Department, Faculty of Chemistry and Biology, University of Santiago of Chile (USACH), Santiago, Chile Western Michigan University, UNITED STATES 2 Environmental Microbiology, Institute of Biosciences, TU Bergakademie Freiberg, Freiberg, Germany |
| AuthorAffiliation_xml | – name: 2 Environmental Microbiology, Institute of Biosciences, TU Bergakademie Freiberg, Freiberg, Germany – name: 1 Biology Department, Faculty of Chemistry and Biology, University of Santiago of Chile (USACH), Santiago, Chile – name: Western Michigan University, UNITED STATES |
| Author_xml | – sequence: 1 givenname: Javier surname: Rivera-Araya fullname: Rivera-Araya, Javier – sequence: 2 givenname: Thomas surname: Heine fullname: Heine, Thomas – sequence: 3 givenname: Renato surname: Chávez fullname: Chávez, Renato – sequence: 4 givenname: Michael surname: Schlömann fullname: Schlömann, Michael – sequence: 5 givenname: Gloria orcidid: 0000-0002-1275-7399 surname: Levicán fullname: Levicán, Gloria |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/35486621$$D View this record in MEDLINE/PubMed |
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| CitedBy_id | crossref_primary_10_3390_min13020243 crossref_primary_10_1016_j_hydromet_2024_106431 |
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| ContentType | Journal Article |
| Copyright | COPYRIGHT 2022 Public Library of Science 2022 Rivera-Araya et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License. 2022 Rivera-Araya et al 2022 Rivera-Araya et al |
| Copyright_xml | – notice: COPYRIGHT 2022 Public Library of Science – notice: 2022 Rivera-Araya et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License. – notice: 2022 Rivera-Araya et al 2022 Rivera-Araya et al |
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| DOI | 10.1371/journal.pone.0267316 |
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| Snippet | Chloride ions are toxic for most acidophilic microorganisms. In this study, the chloride tolerance mechanisms in the acidophilic iron-oxidizing bacterium... |
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| SubjectTerms | Acidification Adaptation Analysis Antioxidants Bacteria Bacteria - genetics Biocompatibility Biology Biology and Life Sciences Biosynthesis Carbonic anhydrase Carbonic anhydrases Chloride Chloride ions Chlorides Cytochrome Cytochrome-c oxidase Cytochromes Data analysis Detoxification Dichloropropane Ectoine Environmental aspects Gene regulation Genes Genetic aspects Genetic transcription Genomics Gram-negative bacteria Halogens Intracellular Iron Lipopolysaccharides Microorganisms Osmotic stress Oxidation Oxygen Oxygen consumption Peptidoglycans Peroxidase Physical Sciences Proteins Protons Quinones Reactive Oxygen Species Reductases Reduction (metal working) Sodium Chloride Solutes Transcriptome Transcriptomics |
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| Title | Transcriptomic analysis of chloride tolerance in Leptospirillum ferriphilum DSM 14647 adapted to NaCl |
| URI | https://www.ncbi.nlm.nih.gov/pubmed/35486621 https://www.proquest.com/docview/2657315380 https://www.proquest.com/docview/2658226467 https://pubmed.ncbi.nlm.nih.gov/PMC9053815 https://doaj.org/article/ce976c163d57457ab4e77d5c9be78721 http://dx.doi.org/10.1371/journal.pone.0267316 |
| Volume | 17 |
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