Production of Acyl-Homoserine Lactone Quorum-Sensing Signals by Gram-Negative Plant-Associated Bacteria
Many gram-negative bacteria regulate expression of specialized gene sets in response to population density. This regulatory mechanism, called autoinduction or quorumsensing, is based on the production by the bacteria of a small, diffusible signal molecule called the autoinducer. In the most well-stu...
| Main Authors: | , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
The American Phytopathological Society
1998-11-01
|
| Series: | Molecular Plant-Microbe Interactions |
| Online Access: | https://apsjournals.apsnet.org/doi/10.1094/MPMI.1998.11.11.1119 |
| _version_ | 1811264531941294080 |
|---|---|
| author | Chung Cha Ping Gao Yu-Ching Chen Paul D. Shaw Stephen K. Farrand |
| author_facet | Chung Cha Ping Gao Yu-Ching Chen Paul D. Shaw Stephen K. Farrand |
| author_sort | Chung Cha |
| collection | DOAJ |
| description | Many gram-negative bacteria regulate expression of specialized gene sets in response to population density. This regulatory mechanism, called autoinduction or quorumsensing, is based on the production by the bacteria of a small, diffusible signal molecule called the autoinducer. In the most well-studied systems the autoinducers are N-acylated derivatives of l-homoserine lactone (acyl-HSL). Signal specificity is conferred by the length, and the nature of the substitution at C-3, of the acyl side-chain. We evaluated four acyl-HSL bioreporters, based on tra of Agrobacterium tumefaciens, lux of Vibrio fischeri, las of Pseudomonas aeruginosa, and pigment production by Chromobacterium violaceum, for their ability to detect sets of 3-oxo acyl-HSLs, 3-hydroxy acyl-HSLs, and alkanoyl-HSLs with chain lengths ranging from C4 to C12. The traG::lacZ fusion reporter from the A. tumefaciens Ti plasmid was the single most sensitive and versatile detector of the four. Using this reporter, we screened 106 isolates representing seven genera of bacteria that associate with plants. Most of the Agrobacterium, Rhizobium, and Pantoea isolates and about half of the Erwinia and Pseudomonas isolates gave positive reactions. Only a few isolates of Xanthomonas produced a detectable signal. We characterized the acyl-HSLs produced by a subset of the isolates by thin-layer chromatography. Among the pseudomonads and erwinias, most produced a single dominant activity chromatographing with the properties of N-(3-oxo-hexanoyl)-l-HSL. However, a few of the erwinias, and the P. fluorescens and Ralstonia solanacearum isolates, produced quite different signals, including 3-hydroxy forms, as well as active compounds that chromatographed with properties unlike any of our standards. The few positive xanthomonads, and almost all of the agrobacteria, produced small amounts of a compound with the chromatographic properties of N-(3-oxo-octanoyl)-l-HSL. Members of the genus Rhizobium showed the greatest diversity, with some producing as few as one and others producing as many as seven detectable signals. Several isolates produced extremely nonpolar compounds indicative of very long acyl side-chains. Production of these compounds suggests that quorum-sensing is common as a gene regulatory mechanism among gram-negative plant-associated bacteria. |
| first_indexed | 2024-04-12T20:06:02Z |
| format | Article |
| id | doaj.art-ade4a59733994be1ac8790dee391feb8 |
| institution | Directory Open Access Journal |
| issn | 0894-0282 1943-7706 |
| language | English |
| last_indexed | 2024-04-12T20:06:02Z |
| publishDate | 1998-11-01 |
| publisher | The American Phytopathological Society |
| record_format | Article |
| series | Molecular Plant-Microbe Interactions |
| spelling | doaj.art-ade4a59733994be1ac8790dee391feb82022-12-22T03:18:24ZengThe American Phytopathological SocietyMolecular Plant-Microbe Interactions0894-02821943-77061998-11-0111111119112910.1094/MPMI.1998.11.11.1119Production of Acyl-Homoserine Lactone Quorum-Sensing Signals by Gram-Negative Plant-Associated BacteriaChung Cha0Ping Gao1Yu-Ching Chen2Paul D. Shaw3Stephen K. Farrand41Department of Crop Sciences, University of Illinois at Urbana-Champaign, Urbana 61801, U.S.A.1Department of Crop Sciences, University of Illinois at Urbana-Champaign, Urbana 61801, U.S.A.1Department of Crop Sciences, University of Illinois at Urbana-Champaign, Urbana 61801, U.S.A.1Department of Crop Sciences, University of Illinois at Urbana-Champaign, Urbana 61801, U.S.A.1Department of Crop Sciences, University of Illinois at Urbana-Champaign, Urbana 61801, U.S.A.Many gram-negative bacteria regulate expression of specialized gene sets in response to population density. This regulatory mechanism, called autoinduction or quorumsensing, is based on the production by the bacteria of a small, diffusible signal molecule called the autoinducer. In the most well-studied systems the autoinducers are N-acylated derivatives of l-homoserine lactone (acyl-HSL). Signal specificity is conferred by the length, and the nature of the substitution at C-3, of the acyl side-chain. We evaluated four acyl-HSL bioreporters, based on tra of Agrobacterium tumefaciens, lux of Vibrio fischeri, las of Pseudomonas aeruginosa, and pigment production by Chromobacterium violaceum, for their ability to detect sets of 3-oxo acyl-HSLs, 3-hydroxy acyl-HSLs, and alkanoyl-HSLs with chain lengths ranging from C4 to C12. The traG::lacZ fusion reporter from the A. tumefaciens Ti plasmid was the single most sensitive and versatile detector of the four. Using this reporter, we screened 106 isolates representing seven genera of bacteria that associate with plants. Most of the Agrobacterium, Rhizobium, and Pantoea isolates and about half of the Erwinia and Pseudomonas isolates gave positive reactions. Only a few isolates of Xanthomonas produced a detectable signal. We characterized the acyl-HSLs produced by a subset of the isolates by thin-layer chromatography. Among the pseudomonads and erwinias, most produced a single dominant activity chromatographing with the properties of N-(3-oxo-hexanoyl)-l-HSL. However, a few of the erwinias, and the P. fluorescens and Ralstonia solanacearum isolates, produced quite different signals, including 3-hydroxy forms, as well as active compounds that chromatographed with properties unlike any of our standards. The few positive xanthomonads, and almost all of the agrobacteria, produced small amounts of a compound with the chromatographic properties of N-(3-oxo-octanoyl)-l-HSL. Members of the genus Rhizobium showed the greatest diversity, with some producing as few as one and others producing as many as seven detectable signals. Several isolates produced extremely nonpolar compounds indicative of very long acyl side-chains. Production of these compounds suggests that quorum-sensing is common as a gene regulatory mechanism among gram-negative plant-associated bacteria.https://apsjournals.apsnet.org/doi/10.1094/MPMI.1998.11.11.1119 |
| spellingShingle | Chung Cha Ping Gao Yu-Ching Chen Paul D. Shaw Stephen K. Farrand Production of Acyl-Homoserine Lactone Quorum-Sensing Signals by Gram-Negative Plant-Associated Bacteria Molecular Plant-Microbe Interactions |
| title | Production of Acyl-Homoserine Lactone Quorum-Sensing Signals by Gram-Negative Plant-Associated Bacteria |
| title_full | Production of Acyl-Homoserine Lactone Quorum-Sensing Signals by Gram-Negative Plant-Associated Bacteria |
| title_fullStr | Production of Acyl-Homoserine Lactone Quorum-Sensing Signals by Gram-Negative Plant-Associated Bacteria |
| title_full_unstemmed | Production of Acyl-Homoserine Lactone Quorum-Sensing Signals by Gram-Negative Plant-Associated Bacteria |
| title_short | Production of Acyl-Homoserine Lactone Quorum-Sensing Signals by Gram-Negative Plant-Associated Bacteria |
| title_sort | production of acyl homoserine lactone quorum sensing signals by gram negative plant associated bacteria |
| url | https://apsjournals.apsnet.org/doi/10.1094/MPMI.1998.11.11.1119 |
| work_keys_str_mv | AT chungcha productionofacylhomoserinelactonequorumsensingsignalsbygramnegativeplantassociatedbacteria AT pinggao productionofacylhomoserinelactonequorumsensingsignalsbygramnegativeplantassociatedbacteria AT yuchingchen productionofacylhomoserinelactonequorumsensingsignalsbygramnegativeplantassociatedbacteria AT pauldshaw productionofacylhomoserinelactonequorumsensingsignalsbygramnegativeplantassociatedbacteria AT stephenkfarrand productionofacylhomoserinelactonequorumsensingsignalsbygramnegativeplantassociatedbacteria |