Detection, Structural Elucidation, and Biological Effects of Diverse N-Acyl-homoserine Lactone Signaling Molecules in the Plant-Promoting Endophytic Bacterium Rhizobium oryzihabitans M15.

Quorum sensing (QS), usually performed by N-acyl-homoserine lactones (AHLs) in Gram-staining-negative bacteria, plays an important role in plant-bacteria interactions. Rhizobium oryzihabitans M15 is a plant-growth-promoting rhizobacterium (PGPR) isolated from rice roots. In this study, we found a QS system in the endogenous plasmid of R. oryzihabitans M15 and detected the activity of AHLs by a bioassay method. We identified five AHL analogues in R. oryzihabitans M15 using liquid chromatography-tandem mass spectrometry (LC-MS). The most dominant AHL analogue was N-(3R-hydroxy-7-cis-tetradecanoyl)-l-homoserine lactone according to nuclear magnetic resonance (NMR) and Mosher's reactions. Furthermore, the rosI mutant abolished AHL production and significantly decreased growth, exopolysaccharide (EPS) production, biofilm formation, and motility compared to the wild-type strain. These results lay the foundation for further investigating the QS regulation mechanism and signal pathway of R. oryzihabitans M15 and its interactions with the host plant.

[1]  Fenglian Fu,et al.  N-Acyl-homoserine lactone-mediated quorum sensing of aerobic granular sludge system in a continuous-flow membrane bioreactor , 2020 .

[2]  Zhihong Xie,et al.  Effects of Calcium and Signal Sensing Systems on Azorhizobium caulinodans Biofilm Formation and Host Colonization , 2020, Frontiers in Microbiology.

[3]  M. Hardt,et al.  The N-acyl homoserine-lactone depleted Rhizobium radiobacter mutant RrF4NM13 shows reduced growth-promoting and resistance-inducing activities in mono- and dicotyledonous plants , 2020, Journal of Plant Diseases and Protection.

[4]  Xueqing Shi,et al.  Analysis of N-Acy-L-homoserine lactones (AHLs) in wastewater treatment systems using SPE-LLE with LC-MS/MS. , 2020, Water research.

[5]  Guishan Zhang,et al.  Isolation, Identification and Characterization of Endophytic Bacterium Rhizobium oryzihabitans sp. nov., from Rice Root with Biotechnological Potential in Agriculture , 2020, Microorganisms.

[6]  W. Ye,et al.  Diketopiperazines synthesis gene in Shewanella baltica and roles of diketopiperazines and resveratrol in quorum sensing. , 2019, Journal of agricultural and food chemistry.

[7]  J. Baldani,et al.  Gluconacetobacter diazotrophicus mitigates drought stress in Oryza sativa L. , 2019, Plant and Soil.

[8]  Dawen Gao,et al.  Specific quorum sensing molecules of ammonia oxidizers and their role during ammonium metabolism in Zhalong wetland, China. , 2019, The Science of the total environment.

[9]  Lihui Liu,et al.  Rhizobium wuzhouense sp. nov., isolated from roots of Oryza officinalis. , 2018, International journal of systematic and evolutionary microbiology.

[10]  M. McIntosh,et al.  Regulation Mediated by N-Acyl Homoserine Lactone Quorum Sensing Signals in the Rhizobium-Legume Symbiosis , 2018, Genes.

[11]  P. Poole,et al.  Rhizobia: from saprophytes to endosymbionts , 2018, Nature Reviews Microbiology.

[12]  Ayesha,et al.  Functional characterization of a soybean growth stimulator Bradyrhizobium sp. strain SR-6 showing acylhomoserine lactone production. , 2016, FEMS microbiology ecology.

[13]  Bonnie L. Bassler,et al.  Quorum sensing signal–response systems in Gram-negative bacteria , 2016, Nature Reviews Microbiology.

[14]  A. Goesmann,et al.  Non-pathogenic Rhizobium radiobacter F4 deploys plant beneficial activity independent of its host Piriformospora indica , 2015, The ISME Journal.

[15]  Lei Zhang,et al.  Rhizobium oryzicola sp. nov., potential plant-growth-promoting endophytic bacteria isolated from rice roots. , 2015, International journal of systematic and evolutionary microbiology.

[16]  J. Schmid,et al.  Methods to identify the unexplored diversity of microbial exopolysaccharides , 2015, Front. Microbiol..

[17]  E. Nester Agrobacterium: nature’s genetic engineer , 2015, Front. Plant Sci..

[18]  W. Giordano,et al.  The Role of Bacterial Biofilms and Surface Components in Plant-Bacterial Associations , 2013, International journal of molecular sciences.

[19]  Fiorela Nievas,et al.  Detection, Characterization, and Biological Effect of Quorum-Sensing Signaling Molecules in Peanut-Nodulating Bradyrhizobia , 2012, Sensors.

[20]  L. Figueroa,et al.  Identification of N-acyl homoserine lactones produced by Gluconacetobacter diazotrophicus PAL5 cultured in complex and synthetic media , 2012, Archives of Microbiology.

[21]  B. Lugtenberg,et al.  Plant-growth-promoting rhizobacteria. , 2009, Annual review of microbiology.

[22]  Jun Zhu,et al.  Exopolysaccharide biosynthesis is important for Mesorhizobium tianshanense: plant host interaction , 2008, Archives of Microbiology.

[23]  T. Cataldi,et al.  Profiling of N-acyl-homoserine lactones by liquid chromatography coupled with electrospray ionization and a hybrid quadrupole linear ion-trap and Fourier-transform ion-cyclotron-resonance mass spectrometry (LC-ESI-LTQ-FTICR-MS). , 2007, Journal of mass spectrometry : JMS.

[24]  A. Hirsch,et al.  Effects of nutritional and environmental conditions on Sinorhizobium meliloti biofilm formation. , 2006, Research in microbiology.

[25]  A. Hirsch,et al.  Investigations of Rhizobium biofilm formation. , 2006, FEMS microbiology ecology.

[26]  R. Pukall,et al.  Discovery of Complex Mixtures of Novel Long‐Chain Quorum Sensing Signals in Free‐Living and Host‐Associated Marine Alphaproteobacteria , 2005, Chembiochem : a European journal of chemical biology.

[27]  M. R. Holden,et al.  Chromosome and plasmid-encoded N-acyl homoserine lactones produced by Agrobacterium vitis wildtype and mutants that differ in their interactions with grape and tobacco , 2005 .

[28]  K. Rolston,et al.  Catheter-Related Bacteremia Caused by Agrobacterium radiobacter in a Cancer Patient: Case Report and Literature Review , 2003, Infection.

[29]  F. Wisniewski-Dyé,et al.  The regulatory locus cinRI in Rhizobium leguminosarum controls a network of quorum‐sensing loci , 2000, Molecular microbiology.

[30]  Roberto Kolter,et al.  Initiation of biofilm formation in Pseudomonas fluorescens WCS365 proceeds via multiple, convergent signalling pathways: a genetic analysis , 1998, Molecular microbiology.

[31]  J. Kijne,et al.  Bacteriocin small of Rhizobium leguminosarum belongs to the class of N-acyl-L-homoserine lactone molecules, known as autoinducers and as quorum sensing co-transcription factors , 1996, Journal of bacteriology.

[32]  T. Kusumi,et al.  A new aspect of the high-field NMR application of Mosher's method. The absolute configuration of marine triterpene sipholenol A , 1991 .

[33]  M. Parsek,et al.  Quorum sensing and microbial biofilms. , 2008, Current topics in microbiology and immunology.