A Diverged Transcriptional Network for Usage of Two Fe-S Cluster Biogenesis Machineries in the Delta-Proteobacterium Myxococcus xanthus
ABSTRACT Myxococcus xanthus possesses two Fe-S cluster biogenesis machineries, ISC (iron-sulfur cluster) and SUF (sulfur mobilization). Here, we show that in comparison to the phylogenetically distant Enterobacteria, which also have both machineries, M. xanthus evolved an independent transcriptional...
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| Format: | Article |
| Language: | English |
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American Society for Microbiology
2023-02-01
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| Series: | mBio |
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| Online Access: | https://journals.asm.org/doi/10.1128/mbio.03001-22 |
| _version_ | 1811163376781361152 |
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| author | Mathieu Sourice Isabel Askenasy Pierre Simon Garcia Yann Denis Gaël Brasseur Patricia J. Kiley Béatrice Py Corinne Aubert |
| author_facet | Mathieu Sourice Isabel Askenasy Pierre Simon Garcia Yann Denis Gaël Brasseur Patricia J. Kiley Béatrice Py Corinne Aubert |
| author_sort | Mathieu Sourice |
| collection | DOAJ |
| description | ABSTRACT Myxococcus xanthus possesses two Fe-S cluster biogenesis machineries, ISC (iron-sulfur cluster) and SUF (sulfur mobilization). Here, we show that in comparison to the phylogenetically distant Enterobacteria, which also have both machineries, M. xanthus evolved an independent transcriptional scheme to coordinately regulate the expression of these machineries. This transcriptional response is directed by RisR, which we show to belong to a phylogenetically distant and biochemically distinct subgroup of the Rrf2 transcription factor family, in comparison to IscR that regulates the isc and suf operons in Enterobacteria. We report that RisR harbors an Fe-S cluster and that holo-RisR acts as a repressor of both the isc and suf operons, in contrast to Escherichia coli, where holo-IscR represses the isc operon whereas apo-IscR activates the suf operon. In addition, we establish that the nature of the cluster and the DNA binding sites of RisR, in the isc and suf operons, diverge from those of IscR. We further show that in M. xanthus, the two machineries appear to be fully interchangeable in maintaining housekeeping levels of Fe-S cluster biogenesis and in synthesizing the Fe-S cluster for their common regulator, RisR. We also demonstrate that in response to oxidative stress and iron limitation, transcriptional upregulation of the M. xanthus isc and suf operons was mediated solely by RisR and that the contribution of the SUF machinery was greater than the ISC machinery. Altogether, these findings shed light on the diversity of homeostatic mechanisms exploited by bacteria to coordinately use two Fe-S cluster biogenesis machineries. IMPORTANCE Fe-S proteins are ubiquitous and control a wide variety of key biological processes; therefore, maintaining Fe-S cluster homeostasis is an essential task for all organisms. Here, we provide the first example of how a bacterium from the Deltaproteobacteria branch coordinates expression of two Fe-S cluster biogenesis machineries. The results revealed a new model of coordination, highlighting the unique and common features that have independently emerged in phylogenetically distant bacteria to maintain Fe-S cluster homeostasis in response to environmental changes. Regulation is orchestrated by a previously uncharacterized transcriptional regulator, RisR, belonging to the Rrf2 superfamily, whose members are known to sense diverse environmental stresses frequently encountered by bacteria. Understanding how M. xanthus maintains Fe-S cluster homeostasis via RisR regulation revealed a strategy reflective of the aerobic lifestyle of this organsim. This new knowledge also paves the way to improve production of Fe-S-dependent secondary metabolites using M. xanthus as a chassis. |
| first_indexed | 2024-04-10T06:44:03Z |
| format | Article |
| id | doaj.art-77a6b1e037b546fd880f4e35e793366b |
| institution | Directory Open Access Journal |
| issn | 2150-7511 |
| language | English |
| last_indexed | 2024-04-10T06:44:03Z |
| publishDate | 2023-02-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | mBio |
| spelling | doaj.art-77a6b1e037b546fd880f4e35e793366b2023-02-28T14:06:24ZengAmerican Society for MicrobiologymBio2150-75112023-02-0114110.1128/mbio.03001-22A Diverged Transcriptional Network for Usage of Two Fe-S Cluster Biogenesis Machineries in the Delta-Proteobacterium Myxococcus xanthusMathieu Sourice0Isabel Askenasy1Pierre Simon Garcia2Yann Denis3Gaël Brasseur4Patricia J. Kiley5Béatrice Py6Corinne Aubert7Laboratoire de Chimie Bactérienne (UMR7283), Institut de Microbiologie de la Méditerranée, Institut Microbiologie Bioénergies et Biotechnologie, Centre National de la Recherche Scientifique, Aix-Marseille Université, Marseille, FranceDepartment of Biomolecular Chemistry, University of Wisconsin–Madison, Madison, Wisconsin, USADepartment of Microbiology, Unit Stress Adaptation and Metabolism in Enterobacteria, Institut Pasteur, Université Paris Cité, Paris, FrancePlate-forme Transcriptomique, Institut de Microbiologie de la Méditerranée (FR3479), Marseille, FranceLaboratoire de Chimie Bactérienne (UMR7283), Institut de Microbiologie de la Méditerranée, Institut Microbiologie Bioénergies et Biotechnologie, Centre National de la Recherche Scientifique, Aix-Marseille Université, Marseille, FranceDepartment of Biomolecular Chemistry, University of Wisconsin–Madison, Madison, Wisconsin, USALaboratoire de Chimie Bactérienne (UMR7283), Institut de Microbiologie de la Méditerranée, Institut Microbiologie Bioénergies et Biotechnologie, Centre National de la Recherche Scientifique, Aix-Marseille Université, Marseille, FranceLaboratoire de Chimie Bactérienne (UMR7283), Institut de Microbiologie de la Méditerranée, Institut Microbiologie Bioénergies et Biotechnologie, Centre National de la Recherche Scientifique, Aix-Marseille Université, Marseille, FranceABSTRACT Myxococcus xanthus possesses two Fe-S cluster biogenesis machineries, ISC (iron-sulfur cluster) and SUF (sulfur mobilization). Here, we show that in comparison to the phylogenetically distant Enterobacteria, which also have both machineries, M. xanthus evolved an independent transcriptional scheme to coordinately regulate the expression of these machineries. This transcriptional response is directed by RisR, which we show to belong to a phylogenetically distant and biochemically distinct subgroup of the Rrf2 transcription factor family, in comparison to IscR that regulates the isc and suf operons in Enterobacteria. We report that RisR harbors an Fe-S cluster and that holo-RisR acts as a repressor of both the isc and suf operons, in contrast to Escherichia coli, where holo-IscR represses the isc operon whereas apo-IscR activates the suf operon. In addition, we establish that the nature of the cluster and the DNA binding sites of RisR, in the isc and suf operons, diverge from those of IscR. We further show that in M. xanthus, the two machineries appear to be fully interchangeable in maintaining housekeeping levels of Fe-S cluster biogenesis and in synthesizing the Fe-S cluster for their common regulator, RisR. We also demonstrate that in response to oxidative stress and iron limitation, transcriptional upregulation of the M. xanthus isc and suf operons was mediated solely by RisR and that the contribution of the SUF machinery was greater than the ISC machinery. Altogether, these findings shed light on the diversity of homeostatic mechanisms exploited by bacteria to coordinately use two Fe-S cluster biogenesis machineries. IMPORTANCE Fe-S proteins are ubiquitous and control a wide variety of key biological processes; therefore, maintaining Fe-S cluster homeostasis is an essential task for all organisms. Here, we provide the first example of how a bacterium from the Deltaproteobacteria branch coordinates expression of two Fe-S cluster biogenesis machineries. The results revealed a new model of coordination, highlighting the unique and common features that have independently emerged in phylogenetically distant bacteria to maintain Fe-S cluster homeostasis in response to environmental changes. Regulation is orchestrated by a previously uncharacterized transcriptional regulator, RisR, belonging to the Rrf2 superfamily, whose members are known to sense diverse environmental stresses frequently encountered by bacteria. Understanding how M. xanthus maintains Fe-S cluster homeostasis via RisR regulation revealed a strategy reflective of the aerobic lifestyle of this organsim. This new knowledge also paves the way to improve production of Fe-S-dependent secondary metabolites using M. xanthus as a chassis.https://journals.asm.org/doi/10.1128/mbio.03001-22Fe-S cluster biogenesisFe-S cluster homeostasisMyxococcus xanthusRrf2-type regulatortranscription regulationoxidative stress |
| spellingShingle | Mathieu Sourice Isabel Askenasy Pierre Simon Garcia Yann Denis Gaël Brasseur Patricia J. Kiley Béatrice Py Corinne Aubert A Diverged Transcriptional Network for Usage of Two Fe-S Cluster Biogenesis Machineries in the Delta-Proteobacterium Myxococcus xanthus mBio Fe-S cluster biogenesis Fe-S cluster homeostasis Myxococcus xanthus Rrf2-type regulator transcription regulation oxidative stress |
| title | A Diverged Transcriptional Network for Usage of Two Fe-S Cluster Biogenesis Machineries in the Delta-Proteobacterium Myxococcus xanthus |
| title_full | A Diverged Transcriptional Network for Usage of Two Fe-S Cluster Biogenesis Machineries in the Delta-Proteobacterium Myxococcus xanthus |
| title_fullStr | A Diverged Transcriptional Network for Usage of Two Fe-S Cluster Biogenesis Machineries in the Delta-Proteobacterium Myxococcus xanthus |
| title_full_unstemmed | A Diverged Transcriptional Network for Usage of Two Fe-S Cluster Biogenesis Machineries in the Delta-Proteobacterium Myxococcus xanthus |
| title_short | A Diverged Transcriptional Network for Usage of Two Fe-S Cluster Biogenesis Machineries in the Delta-Proteobacterium Myxococcus xanthus |
| title_sort | diverged transcriptional network for usage of two fe s cluster biogenesis machineries in the delta proteobacterium myxococcus xanthus |
| topic | Fe-S cluster biogenesis Fe-S cluster homeostasis Myxococcus xanthus Rrf2-type regulator transcription regulation oxidative stress |
| url | https://journals.asm.org/doi/10.1128/mbio.03001-22 |
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