Interkingdom Signaling of the Insect Pathogen <i>Photorhabdus luminescens</i> with Plants Via the LuxR solo SdiA
In bacteria, group-coordinated behavior such as biofilm formation or virulence are often mediated via cell–cell communication, a process referred to as quorum sensing (QS). The canonical QS system of Gram-negative bacteria uses <i>N</i>-acyl homoserine lactones (AHLs) as communication mo...
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| Format: | Article |
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MDPI AG
2023-03-01
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| Series: | Microorganisms |
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| Online Access: | https://www.mdpi.com/2076-2607/11/4/890 |
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| author | Nazzareno Dominelli Alice Regaiolo Leon Willy Ralf Heermann |
| author_facet | Nazzareno Dominelli Alice Regaiolo Leon Willy Ralf Heermann |
| author_sort | Nazzareno Dominelli |
| collection | DOAJ |
| description | In bacteria, group-coordinated behavior such as biofilm formation or virulence are often mediated via cell–cell communication, a process referred to as quorum sensing (QS). The canonical QS system of Gram-negative bacteria uses <i>N</i>-acyl homoserine lactones (AHLs) as communication molecules, which are produced by LuxI-type synthases and sensed by cognate LuxR-type receptors. These receptors act as transcriptional regulators controlling the expression of specific genes. Some bacteria harbor LuxR-type receptors lacking a cognate LuxI-type synthases, designated as LuxR solos. Among many other LuxR solos, the entomopathogenic enteric bacterium <i>Photorhabdus luminescens</i> harbors a SdiA-like LuxR solo containing an AHL signal-binding domain, for which a respective signal molecule and target genes have not been identified yet. Here we performed SPR analysis to demonstrate that SdiA acts as a bidirectional regulator of transcription, tightly controlling its own expression and the adjacent <i>PluDJC_01670</i> (<i>aidA</i>) gene in <i>P. luminescens,</i> a gene supposed to be involved in the colonization of eukaryotes. Via qPCR we could further determine that in <i>sdiA</i> deletion mutant strains, <i>aidA</i> is upregulated, indicating that SdiA negatively affects expression of <i>aidA</i>. Furthermore, the Δ<i>sdiA</i> deletion mutant exhibited differences in biofilm formation and motility compared with the wild-type. Finally, using nanoDSF analysis we could identify putative binding ability of SdiA towards diverse AHLs, but also to plant-derived signals, modulating the DNA-binding capacity of SdiA, suggesting that this LuxR solo acts as an important player in interkingdom signaling between <i>P. luminescens</i> and plants. |
| first_indexed | 2024-03-11T04:43:33Z |
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| institution | Directory Open Access Journal |
| issn | 2076-2607 |
| language | English |
| last_indexed | 2024-03-11T04:43:33Z |
| publishDate | 2023-03-01 |
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| spelling | doaj.art-6ca403b2beac4399a80fb7a54ba578f82023-11-17T20:32:01ZengMDPI AGMicroorganisms2076-26072023-03-0111489010.3390/microorganisms11040890Interkingdom Signaling of the Insect Pathogen <i>Photorhabdus luminescens</i> with Plants Via the LuxR solo SdiANazzareno Dominelli0Alice Regaiolo1Leon Willy2Ralf Heermann3Institute of Molecular Physiology (imP), Johannes-Gutenberg-University Mainz, Biocenter II, Microbiology and Biotechnology, Hanns-Dieter-Hüsch-Weg 17, 55128 Mainz, GermanyInstitute of Molecular Physiology (imP), Johannes-Gutenberg-University Mainz, Biocenter II, Microbiology and Biotechnology, Hanns-Dieter-Hüsch-Weg 17, 55128 Mainz, GermanyInstitute of Molecular Physiology (imP), Johannes-Gutenberg-University Mainz, Biocenter II, Microbiology and Biotechnology, Hanns-Dieter-Hüsch-Weg 17, 55128 Mainz, GermanyInstitute of Molecular Physiology (imP), Johannes-Gutenberg-University Mainz, Biocenter II, Microbiology and Biotechnology, Hanns-Dieter-Hüsch-Weg 17, 55128 Mainz, GermanyIn bacteria, group-coordinated behavior such as biofilm formation or virulence are often mediated via cell–cell communication, a process referred to as quorum sensing (QS). The canonical QS system of Gram-negative bacteria uses <i>N</i>-acyl homoserine lactones (AHLs) as communication molecules, which are produced by LuxI-type synthases and sensed by cognate LuxR-type receptors. These receptors act as transcriptional regulators controlling the expression of specific genes. Some bacteria harbor LuxR-type receptors lacking a cognate LuxI-type synthases, designated as LuxR solos. Among many other LuxR solos, the entomopathogenic enteric bacterium <i>Photorhabdus luminescens</i> harbors a SdiA-like LuxR solo containing an AHL signal-binding domain, for which a respective signal molecule and target genes have not been identified yet. Here we performed SPR analysis to demonstrate that SdiA acts as a bidirectional regulator of transcription, tightly controlling its own expression and the adjacent <i>PluDJC_01670</i> (<i>aidA</i>) gene in <i>P. luminescens,</i> a gene supposed to be involved in the colonization of eukaryotes. Via qPCR we could further determine that in <i>sdiA</i> deletion mutant strains, <i>aidA</i> is upregulated, indicating that SdiA negatively affects expression of <i>aidA</i>. Furthermore, the Δ<i>sdiA</i> deletion mutant exhibited differences in biofilm formation and motility compared with the wild-type. Finally, using nanoDSF analysis we could identify putative binding ability of SdiA towards diverse AHLs, but also to plant-derived signals, modulating the DNA-binding capacity of SdiA, suggesting that this LuxR solo acts as an important player in interkingdom signaling between <i>P. luminescens</i> and plants.https://www.mdpi.com/2076-2607/11/4/890entomopathogenic bacteriaquorum sensingbacteria–plant interactionAidALuxR-type receptor |
| spellingShingle | Nazzareno Dominelli Alice Regaiolo Leon Willy Ralf Heermann Interkingdom Signaling of the Insect Pathogen <i>Photorhabdus luminescens</i> with Plants Via the LuxR solo SdiA Microorganisms entomopathogenic bacteria quorum sensing bacteria–plant interaction AidA LuxR-type receptor |
| title | Interkingdom Signaling of the Insect Pathogen <i>Photorhabdus luminescens</i> with Plants Via the LuxR solo SdiA |
| title_full | Interkingdom Signaling of the Insect Pathogen <i>Photorhabdus luminescens</i> with Plants Via the LuxR solo SdiA |
| title_fullStr | Interkingdom Signaling of the Insect Pathogen <i>Photorhabdus luminescens</i> with Plants Via the LuxR solo SdiA |
| title_full_unstemmed | Interkingdom Signaling of the Insect Pathogen <i>Photorhabdus luminescens</i> with Plants Via the LuxR solo SdiA |
| title_short | Interkingdom Signaling of the Insect Pathogen <i>Photorhabdus luminescens</i> with Plants Via the LuxR solo SdiA |
| title_sort | interkingdom signaling of the insect pathogen i photorhabdus luminescens i with plants via the luxr solo sdia |
| topic | entomopathogenic bacteria quorum sensing bacteria–plant interaction AidA LuxR-type receptor |
| url | https://www.mdpi.com/2076-2607/11/4/890 |
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