Unravelling HetC as a peptidase-based ABC exporter driving functional cell differentiation in the cyanobacterium Nostoc PCC 7120
ABSTRACTThe export of peptides or proteins is essential for a variety of important functions in bacteria. Among the diverse protein-translocation systems, peptidase-containing ABC transporters (PCAT) are involved in the maturation and export of quorum-sensing or antimicrobial peptides in Gram-positi...
| Main Authors: | , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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American Society for Microbiology
2024-04-01
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| Series: | Microbiology Spectrum |
| Subjects: | |
| Online Access: | https://journals.asm.org/doi/10.1128/spectrum.04058-23 |
| _version_ | 1797228825855131648 |
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| author | Raphaël Rachedi Véronique Risoul Maryline Foglino Yanis Aoudache Kevin Lang Stéphanie Champ Elise Kaplan Cédric Orelle Badreddine Douzi Jean-Michel Jault Amel Latifi |
| author_facet | Raphaël Rachedi Véronique Risoul Maryline Foglino Yanis Aoudache Kevin Lang Stéphanie Champ Elise Kaplan Cédric Orelle Badreddine Douzi Jean-Michel Jault Amel Latifi |
| author_sort | Raphaël Rachedi |
| collection | DOAJ |
| description | ABSTRACTThe export of peptides or proteins is essential for a variety of important functions in bacteria. Among the diverse protein-translocation systems, peptidase-containing ABC transporters (PCAT) are involved in the maturation and export of quorum-sensing or antimicrobial peptides in Gram-positive bacteria and of toxins in Gram-negative organisms. In the multicellular and diazotrophic cyanobacterium Nostoc PCC 7120, the protein HetC is essential for the differentiation of functional heterocysts, which are micro-oxic and non-dividing cells specialized in atmospheric nitrogen fixation. HetC shows similarities to PCAT systems, but whether it actually acts as a peptidase-based exporter remains to be established. In this study, we show that the N-terminal part of HetC, encompassing the peptidase domain, displays a cysteine-type protease activity. The conserved catalytic residues conserved in this family of proteases are essential for the proteolytic activity of HetC and the differentiation of heterocysts. Furthermore, we show that the catalytic residue of the ATPase domain of HetC is also essential for cell differentiation. Interestingly, HetC has a cyclic nucleotide-binding domain at its N-terminus which can bind ppGpp in vitro and which is required for its function in vivo. Our results indicate that HetC is a peculiar PCAT that might be regulated by ppGpp to potentially facilitate the export of a signaling peptide essential for cell differentiation, thereby broadening the scope of PCAT role in Gram-negative bacteria.IMPORTANCEBacteria have a great capacity to adapt to various environmental and physiological conditions; it is widely accepted that their ability to produce extracellular molecules contributes greatly to their fitness. Exported molecules are used for a variety of purposes ranging from communication to adjust cellular physiology, to the production of toxins that bacteria secrete to fight for their ecological niche. They use export machineries for this purpose, the most common of which energize transport by hydrolysis of adenosine triphosphate. Here, we demonstrate that such a mechanism is involved in cell differentiation in the filamentous cyanobacterium Nostoc PCC 7120. The HetC protein belongs to the ATP-binding cassette transporter superfamily and presumably ensures the maturation of a yet unknown substrate during export. These results open interesting perspectives on cellular signaling pathways involving the export of regulatory peptides, which will broaden our knowledge of how these bacteria use two cell types to conciliate photosynthesis and nitrogen fixation. |
| first_indexed | 2024-04-24T15:02:51Z |
| format | Article |
| id | doaj.art-2b8bae40e7154bb5b13bb5283dfaecd0 |
| institution | Directory Open Access Journal |
| issn | 2165-0497 |
| language | English |
| last_indexed | 2024-04-24T15:02:51Z |
| publishDate | 2024-04-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | Microbiology Spectrum |
| spelling | doaj.art-2b8bae40e7154bb5b13bb5283dfaecd02024-04-02T14:16:18ZengAmerican Society for MicrobiologyMicrobiology Spectrum2165-04972024-04-0112410.1128/spectrum.04058-23Unravelling HetC as a peptidase-based ABC exporter driving functional cell differentiation in the cyanobacterium Nostoc PCC 7120Raphaël Rachedi0Véronique Risoul1Maryline Foglino2Yanis Aoudache3Kevin Lang4Stéphanie Champ5Elise Kaplan6Cédric Orelle7Badreddine Douzi8Jean-Michel Jault9Amel Latifi10Aix-Marseille Université, CNRS, Laboratoire de Chimie Bactérienne LCB, IMM, Marseille, FranceAix-Marseille Université, CNRS, Laboratoire de Chimie Bactérienne LCB, IMM, Marseille, FranceAix-Marseille Université, CNRS, Laboratoire de Chimie Bactérienne LCB, IMM, Marseille, FranceUniversité de Lorraine, INRAE, DynAMic, Nancy, FranceMicrobiologie Moléculaire et Biochimie Structurale, UMR5086 Université de Lyon/CNRS, IBCP, Lyon, FranceAix-Marseille Université, CNRS, Laboratoire de Chimie Bactérienne LCB, IMM, Marseille, FranceMicrobiologie Moléculaire et Biochimie Structurale, UMR5086 Université de Lyon/CNRS, IBCP, Lyon, FranceMicrobiologie Moléculaire et Biochimie Structurale, UMR5086 Université de Lyon/CNRS, IBCP, Lyon, FranceUniversité de Lorraine, INRAE, DynAMic, Nancy, FranceMicrobiologie Moléculaire et Biochimie Structurale, UMR5086 Université de Lyon/CNRS, IBCP, Lyon, FranceAix-Marseille Université, CNRS, Laboratoire de Chimie Bactérienne LCB, IMM, Marseille, FranceABSTRACTThe export of peptides or proteins is essential for a variety of important functions in bacteria. Among the diverse protein-translocation systems, peptidase-containing ABC transporters (PCAT) are involved in the maturation and export of quorum-sensing or antimicrobial peptides in Gram-positive bacteria and of toxins in Gram-negative organisms. In the multicellular and diazotrophic cyanobacterium Nostoc PCC 7120, the protein HetC is essential for the differentiation of functional heterocysts, which are micro-oxic and non-dividing cells specialized in atmospheric nitrogen fixation. HetC shows similarities to PCAT systems, but whether it actually acts as a peptidase-based exporter remains to be established. In this study, we show that the N-terminal part of HetC, encompassing the peptidase domain, displays a cysteine-type protease activity. The conserved catalytic residues conserved in this family of proteases are essential for the proteolytic activity of HetC and the differentiation of heterocysts. Furthermore, we show that the catalytic residue of the ATPase domain of HetC is also essential for cell differentiation. Interestingly, HetC has a cyclic nucleotide-binding domain at its N-terminus which can bind ppGpp in vitro and which is required for its function in vivo. Our results indicate that HetC is a peculiar PCAT that might be regulated by ppGpp to potentially facilitate the export of a signaling peptide essential for cell differentiation, thereby broadening the scope of PCAT role in Gram-negative bacteria.IMPORTANCEBacteria have a great capacity to adapt to various environmental and physiological conditions; it is widely accepted that their ability to produce extracellular molecules contributes greatly to their fitness. Exported molecules are used for a variety of purposes ranging from communication to adjust cellular physiology, to the production of toxins that bacteria secrete to fight for their ecological niche. They use export machineries for this purpose, the most common of which energize transport by hydrolysis of adenosine triphosphate. Here, we demonstrate that such a mechanism is involved in cell differentiation in the filamentous cyanobacterium Nostoc PCC 7120. The HetC protein belongs to the ATP-binding cassette transporter superfamily and presumably ensures the maturation of a yet unknown substrate during export. These results open interesting perspectives on cellular signaling pathways involving the export of regulatory peptides, which will broaden our knowledge of how these bacteria use two cell types to conciliate photosynthesis and nitrogen fixation.https://journals.asm.org/doi/10.1128/spectrum.04058-23ABC-transportercyanobacteriagene regulationheterocyst differentiationpeptidasePCAT |
| spellingShingle | Raphaël Rachedi Véronique Risoul Maryline Foglino Yanis Aoudache Kevin Lang Stéphanie Champ Elise Kaplan Cédric Orelle Badreddine Douzi Jean-Michel Jault Amel Latifi Unravelling HetC as a peptidase-based ABC exporter driving functional cell differentiation in the cyanobacterium Nostoc PCC 7120 Microbiology Spectrum ABC-transporter cyanobacteria gene regulation heterocyst differentiation peptidase PCAT |
| title | Unravelling HetC as a peptidase-based ABC exporter driving functional cell differentiation in the cyanobacterium Nostoc PCC 7120 |
| title_full | Unravelling HetC as a peptidase-based ABC exporter driving functional cell differentiation in the cyanobacterium Nostoc PCC 7120 |
| title_fullStr | Unravelling HetC as a peptidase-based ABC exporter driving functional cell differentiation in the cyanobacterium Nostoc PCC 7120 |
| title_full_unstemmed | Unravelling HetC as a peptidase-based ABC exporter driving functional cell differentiation in the cyanobacterium Nostoc PCC 7120 |
| title_short | Unravelling HetC as a peptidase-based ABC exporter driving functional cell differentiation in the cyanobacterium Nostoc PCC 7120 |
| title_sort | unravelling hetc as a peptidase based abc exporter driving functional cell differentiation in the cyanobacterium nostoc pcc 7120 |
| topic | ABC-transporter cyanobacteria gene regulation heterocyst differentiation peptidase PCAT |
| url | https://journals.asm.org/doi/10.1128/spectrum.04058-23 |
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