Tolerance to alkaline ambient pH in Aspergillus nidulans depends on the activity of ENA proteins
Tolerance of microorganisms to abiotic stress is enabled by regulatory mechanisms that coordinate the expression and activity of resistance genes. Alkalinity and high salt concentrations are major environmental physicochemical stresses. Here, we analyzed the roles of sodium-extrusion family (ENA) tr...
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Published in | Scientific reports Vol. 10; no. 1; p. 14325 |
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Main Authors | , , , , |
Format | Journal Article |
Language | English |
Published |
London
Nature Publishing Group UK
31.08.2020
Nature Publishing Group |
Subjects | |
Online Access | Get full text |
ISSN | 2045-2322 2045-2322 |
DOI | 10.1038/s41598-020-71297-z |
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Abstract | Tolerance of microorganisms to abiotic stress is enabled by regulatory mechanisms that coordinate the expression and activity of resistance genes. Alkalinity and high salt concentrations are major environmental physicochemical stresses. Here, we analyzed the roles of sodium-extrusion family (ENA) transporters EnaA, EnaB and EnaC in the response to these stress conditions in the filamentous fungus
Aspergillus nidulans
. While EnaC has a minor role, EnaB is a key element for tolerance to Na
+
and Li
+
toxicity. Adaptation to alkaline pH requires the concerted action of EnaB with EnaA. Accordingly, expression of
enaA
and
enaB
was induced by Na
+
, Li
+
and pH 8. These expression patterns are altered in a
sltA
Δ background and completely inhibited in a mutant expressing non-functional PacC protein (
palH72
). However, a constitutively active PacC form was not sufficient to restore maximum
enaA
expression. In agreement with their predicted role as membrane ATPases, EnaA localized to the plasma membrane while EnaB accumulated at structures resembling the endoplasmic reticulum. Overall, results suggest different PacC- and SltA-dependent roles for EnaB in pH and salt homeostasis, acting in coordination with EnaA at pH 8 but independently under salt stress. |
---|---|
AbstractList | Tolerance of microorganisms to abiotic stress is enabled by regulatory mechanisms that coordinate the expression and activity of resistance genes. Alkalinity and high salt concentrations are major environmental physicochemical stresses. Here, we analyzed the roles of sodium-extrusion family (ENA) transporters EnaA, EnaB and EnaC in the response to these stress conditions in the filamentous fungus Aspergillus nidulans. While EnaC has a minor role, EnaB is a key element for tolerance to Na+ and Li+ toxicity. Adaptation to alkaline pH requires the concerted action of EnaB with EnaA. Accordingly, expression of enaA and enaB was induced by Na+, Li+ and pH 8. These expression patterns are altered in a sltAΔ background and completely inhibited in a mutant expressing non-functional PacC protein (palH72). However, a constitutively active PacC form was not sufficient to restore maximum enaA expression. In agreement with their predicted role as membrane ATPases, EnaA localized to the plasma membrane while EnaB accumulated at structures resembling the endoplasmic reticulum. Overall, results suggest different PacC- and SltA-dependent roles for EnaB in pH and salt homeostasis, acting in coordination with EnaA at pH 8 but independently under salt stress. Tolerance of microorganisms to abiotic stress is enabled by regulatory mechanisms that coordinate the expression and activity of resistance genes. Alkalinity and high salt concentrations are major environmental physicochemical stresses. Here, we analyzed the roles of sodium-extrusion family (ENA) transporters EnaA, EnaB and EnaC in the response to these stress conditions in the filamentous fungus Aspergillus nidulans. While EnaC has a minor role, EnaB is a key element for tolerance to Na+ and Li+ toxicity. Adaptation to alkaline pH requires the concerted action of EnaB with EnaA. Accordingly, expression of enaA and enaB was induced by Na+, Li+ and pH 8. These expression patterns are altered in a sltAΔ background and completely inhibited in a mutant expressing non-functional PacC protein (palH72). However, a constitutively active PacC form was not sufficient to restore maximum enaA expression. In agreement with their predicted role as membrane ATPases, EnaA localized to the plasma membrane while EnaB accumulated at structures resembling the endoplasmic reticulum. Overall, results suggest different PacC- and SltA-dependent roles for EnaB in pH and salt homeostasis, acting in coordination with EnaA at pH 8 but independently under salt stress.Tolerance of microorganisms to abiotic stress is enabled by regulatory mechanisms that coordinate the expression and activity of resistance genes. Alkalinity and high salt concentrations are major environmental physicochemical stresses. Here, we analyzed the roles of sodium-extrusion family (ENA) transporters EnaA, EnaB and EnaC in the response to these stress conditions in the filamentous fungus Aspergillus nidulans. While EnaC has a minor role, EnaB is a key element for tolerance to Na+ and Li+ toxicity. Adaptation to alkaline pH requires the concerted action of EnaB with EnaA. Accordingly, expression of enaA and enaB was induced by Na+, Li+ and pH 8. These expression patterns are altered in a sltAΔ background and completely inhibited in a mutant expressing non-functional PacC protein (palH72). However, a constitutively active PacC form was not sufficient to restore maximum enaA expression. In agreement with their predicted role as membrane ATPases, EnaA localized to the plasma membrane while EnaB accumulated at structures resembling the endoplasmic reticulum. Overall, results suggest different PacC- and SltA-dependent roles for EnaB in pH and salt homeostasis, acting in coordination with EnaA at pH 8 but independently under salt stress. Tolerance of microorganisms to abiotic stress is enabled by regulatory mechanisms that coordinate the expression and activity of resistance genes. Alkalinity and high salt concentrations are major environmental physicochemical stresses. Here, we analyzed the roles of sodium-extrusion family (ENA) transporters EnaA, EnaB and EnaC in the response to these stress conditions in the filamentous fungus Aspergillus nidulans. While EnaC has a minor role, EnaB is a key element for tolerance to Na and Li toxicity. Adaptation to alkaline pH requires the concerted action of EnaB with EnaA. Accordingly, expression of enaA and enaB was induced by Na , Li and pH 8. These expression patterns are altered in a sltAΔ background and completely inhibited in a mutant expressing non-functional PacC protein (palH72). However, a constitutively active PacC form was not sufficient to restore maximum enaA expression. In agreement with their predicted role as membrane ATPases, EnaA localized to the plasma membrane while EnaB accumulated at structures resembling the endoplasmic reticulum. Overall, results suggest different PacC- and SltA-dependent roles for EnaB in pH and salt homeostasis, acting in coordination with EnaA at pH 8 but independently under salt stress. Tolerance of microorganisms to abiotic stress is enabled by regulatory mechanisms that coordinate the expression and activity of resistance genes. Alkalinity and high salt concentrations are major environmental physicochemical stresses. Here, we analyzed the roles of sodium-extrusion family (ENA) transporters EnaA, EnaB and EnaC in the response to these stress conditions in the filamentous fungus Aspergillus nidulans . While EnaC has a minor role, EnaB is a key element for tolerance to Na + and Li + toxicity. Adaptation to alkaline pH requires the concerted action of EnaB with EnaA. Accordingly, expression of enaA and enaB was induced by Na + , Li + and pH 8. These expression patterns are altered in a sltA Δ background and completely inhibited in a mutant expressing non-functional PacC protein ( palH72 ). However, a constitutively active PacC form was not sufficient to restore maximum enaA expression. In agreement with their predicted role as membrane ATPases, EnaA localized to the plasma membrane while EnaB accumulated at structures resembling the endoplasmic reticulum. Overall, results suggest different PacC- and SltA-dependent roles for EnaB in pH and salt homeostasis, acting in coordination with EnaA at pH 8 but independently under salt stress. |
ArticleNumber | 14325 |
Author | Espeso, Eduardo A. Etxebeste, Oier Spielvogel, Anja Markina-Iñarrairaegui, Ane Ugalde, Unai |
Author_xml | – sequence: 1 givenname: Ane surname: Markina-Iñarrairaegui fullname: Markina-Iñarrairaegui, Ane organization: Department of Applied Chemistry, Faculty of Chemistry, University of the Basque Country – sequence: 2 givenname: Anja surname: Spielvogel fullname: Spielvogel, Anja organization: Department of Cellular and Molecular Medicine, Centro de Investigaciones Biológicas Margarita Salas, C.S.I.C – sequence: 3 givenname: Oier orcidid: 0000-0002-9786-6091 surname: Etxebeste fullname: Etxebeste, Oier organization: Department of Applied Chemistry, Faculty of Chemistry, University of the Basque Country – sequence: 4 givenname: Unai surname: Ugalde fullname: Ugalde, Unai organization: Department of Applied Chemistry, Faculty of Chemistry, University of the Basque Country – sequence: 5 givenname: Eduardo A. orcidid: 0000-0002-5873-6059 surname: Espeso fullname: Espeso, Eduardo A. email: eespeso@cib.csic.es organization: Department of Cellular and Molecular Medicine, Centro de Investigaciones Biológicas Margarita Salas, C.S.I.C |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/32868868$$D View this record in MEDLINE/PubMed |
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Snippet | Tolerance of microorganisms to abiotic stress is enabled by regulatory mechanisms that coordinate the expression and activity of resistance genes. Alkalinity... |
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SubjectTerms | 631/326/325/1507 631/326/88 Adenosine Triphosphatases - genetics Adenosine Triphosphatases - metabolism Algae Alkalinity Aspergillus nidulans - genetics Aspergillus nidulans - metabolism Cation Transport Proteins - genetics Cation Transport Proteins - metabolism Cell division Flowering Fungal Proteins - metabolism Gene Expression Regulation Humanities and Social Sciences Hydrogen-Ion Concentration Isoetes Lithium - metabolism Microorganisms multidisciplinary Phylogeny Salt Tolerance Salts Science Science (multidisciplinary) Sodium - metabolism Transcription Factors - metabolism |
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Title | Tolerance to alkaline ambient pH in Aspergillus nidulans depends on the activity of ENA proteins |
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