Adaptation of <i>Cupriavidus metallidurans</i> CH34 to Toxic Zinc Concentrations Involves an Uncharacterized ABC-Type Transporter
<i>Cupriavidus metallidurans</i> CH34 is a well-studied metal-resistant β-proteobacterium and contains a battery of genes participating in metal metabolism and resistance. Here, we generated a mutant (CH34<sup>ZnR</sup>) adapted to high zinc concentrations in order to study h...
| Main Authors: | , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
MDPI AG
2021-02-01
|
| Series: | Microorganisms |
| Subjects: | |
| Online Access: | https://www.mdpi.com/2076-2607/9/2/309 |
| _version_ | 1797416545385709568 |
|---|---|
| author | Rob Van Houdt Joachim Vandecraen Natalie Leys Pieter Monsieurs Abram Aertsen |
| author_facet | Rob Van Houdt Joachim Vandecraen Natalie Leys Pieter Monsieurs Abram Aertsen |
| author_sort | Rob Van Houdt |
| collection | DOAJ |
| description | <i>Cupriavidus metallidurans</i> CH34 is a well-studied metal-resistant β-proteobacterium and contains a battery of genes participating in metal metabolism and resistance. Here, we generated a mutant (CH34<sup>ZnR</sup>) adapted to high zinc concentrations in order to study how CH34 could adaptively further increase its resistance against this metal. Characterization of CH34<sup>ZnR</sup> revealed that it was also more resistant to cadmium, and that it incurred seven insertion sequence-mediated mutations. Among these, an IS<i>1088</i> disruption of the <i>glpR</i> gene (encoding a DeoR-type transcriptional repressor) resulted in the constitutive expression of the neighboring ATP-binding cassette (ABC)-type transporter. GlpR and the adjacent ABC transporter are highly similar to the glycerol operon regulator and ATP-driven glycerol importer of <i>Rhizobium leguminosarum</i> bv. <i>viciae</i> VF39, respectively. Deletion of <i>glpR</i> or the ABC transporter and complementation of CH34<sup>ZnR</sup> with the parental <i>glpR</i> gene further demonstrated that loss of GlpR function and concomitant derepression of the adjacent ABC transporter is pivotal for the observed resistance phenotype. Importantly, addition of glycerol, presumably by glycerol-mediated attenuation of GlpR activity, also promoted increased zinc and cadmium resistance in the parental CH34 strain. Upregulation of this ABC-type transporter is therefore proposed as a new adaptation route towards metal resistance. |
| first_indexed | 2024-03-09T06:04:48Z |
| format | Article |
| id | doaj.art-d5ca5d93a9da416ba016671ec5aa2e00 |
| institution | Directory Open Access Journal |
| issn | 2076-2607 |
| language | English |
| last_indexed | 2024-03-09T06:04:48Z |
| publishDate | 2021-02-01 |
| publisher | MDPI AG |
| record_format | Article |
| series | Microorganisms |
| spelling | doaj.art-d5ca5d93a9da416ba016671ec5aa2e002023-12-03T12:05:13ZengMDPI AGMicroorganisms2076-26072021-02-019230910.3390/microorganisms9020309Adaptation of <i>Cupriavidus metallidurans</i> CH34 to Toxic Zinc Concentrations Involves an Uncharacterized ABC-Type TransporterRob Van Houdt0Joachim Vandecraen1Natalie Leys2Pieter Monsieurs3Abram Aertsen4Microbiology Unit, Interdisciplinary Biosciences, Belgian Nuclear Research Centre (SCK CEN), 2400 Mol, BelgiumMicrobiology Unit, Interdisciplinary Biosciences, Belgian Nuclear Research Centre (SCK CEN), 2400 Mol, BelgiumMicrobiology Unit, Interdisciplinary Biosciences, Belgian Nuclear Research Centre (SCK CEN), 2400 Mol, BelgiumMicrobiology Unit, Interdisciplinary Biosciences, Belgian Nuclear Research Centre (SCK CEN), 2400 Mol, BelgiumLaboratory of Food Microbiology, Department of Microbial and Molecular Systems, Faculty of Bioscience Engineering, Katholieke Universiteit Leuven, 3000 Leuven, Belgium<i>Cupriavidus metallidurans</i> CH34 is a well-studied metal-resistant β-proteobacterium and contains a battery of genes participating in metal metabolism and resistance. Here, we generated a mutant (CH34<sup>ZnR</sup>) adapted to high zinc concentrations in order to study how CH34 could adaptively further increase its resistance against this metal. Characterization of CH34<sup>ZnR</sup> revealed that it was also more resistant to cadmium, and that it incurred seven insertion sequence-mediated mutations. Among these, an IS<i>1088</i> disruption of the <i>glpR</i> gene (encoding a DeoR-type transcriptional repressor) resulted in the constitutive expression of the neighboring ATP-binding cassette (ABC)-type transporter. GlpR and the adjacent ABC transporter are highly similar to the glycerol operon regulator and ATP-driven glycerol importer of <i>Rhizobium leguminosarum</i> bv. <i>viciae</i> VF39, respectively. Deletion of <i>glpR</i> or the ABC transporter and complementation of CH34<sup>ZnR</sup> with the parental <i>glpR</i> gene further demonstrated that loss of GlpR function and concomitant derepression of the adjacent ABC transporter is pivotal for the observed resistance phenotype. Importantly, addition of glycerol, presumably by glycerol-mediated attenuation of GlpR activity, also promoted increased zinc and cadmium resistance in the parental CH34 strain. Upregulation of this ABC-type transporter is therefore proposed as a new adaptation route towards metal resistance.https://www.mdpi.com/2076-2607/9/2/309<i>Cupriavidus metallidurans</i>zinc resistancecadmium resistancedirected evolutionABC transporter |
| spellingShingle | Rob Van Houdt Joachim Vandecraen Natalie Leys Pieter Monsieurs Abram Aertsen Adaptation of <i>Cupriavidus metallidurans</i> CH34 to Toxic Zinc Concentrations Involves an Uncharacterized ABC-Type Transporter Microorganisms <i>Cupriavidus metallidurans</i> zinc resistance cadmium resistance directed evolution ABC transporter |
| title | Adaptation of <i>Cupriavidus metallidurans</i> CH34 to Toxic Zinc Concentrations Involves an Uncharacterized ABC-Type Transporter |
| title_full | Adaptation of <i>Cupriavidus metallidurans</i> CH34 to Toxic Zinc Concentrations Involves an Uncharacterized ABC-Type Transporter |
| title_fullStr | Adaptation of <i>Cupriavidus metallidurans</i> CH34 to Toxic Zinc Concentrations Involves an Uncharacterized ABC-Type Transporter |
| title_full_unstemmed | Adaptation of <i>Cupriavidus metallidurans</i> CH34 to Toxic Zinc Concentrations Involves an Uncharacterized ABC-Type Transporter |
| title_short | Adaptation of <i>Cupriavidus metallidurans</i> CH34 to Toxic Zinc Concentrations Involves an Uncharacterized ABC-Type Transporter |
| title_sort | adaptation of i cupriavidus metallidurans i ch34 to toxic zinc concentrations involves an uncharacterized abc type transporter |
| topic | <i>Cupriavidus metallidurans</i> zinc resistance cadmium resistance directed evolution ABC transporter |
| url | https://www.mdpi.com/2076-2607/9/2/309 |
| work_keys_str_mv | AT robvanhoudt adaptationoficupriavidusmetalliduransich34totoxiczincconcentrationsinvolvesanuncharacterizedabctypetransporter AT joachimvandecraen adaptationoficupriavidusmetalliduransich34totoxiczincconcentrationsinvolvesanuncharacterizedabctypetransporter AT natalieleys adaptationoficupriavidusmetalliduransich34totoxiczincconcentrationsinvolvesanuncharacterizedabctypetransporter AT pietermonsieurs adaptationoficupriavidusmetalliduransich34totoxiczincconcentrationsinvolvesanuncharacterizedabctypetransporter AT abramaertsen adaptationoficupriavidusmetalliduransich34totoxiczincconcentrationsinvolvesanuncharacterizedabctypetransporter |