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Production of Acyl-Homoserine Lactone Quorum-Sensing Signals Is Wide- Spread in Gram-Negative Methylobacterium

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Production of Acyl-Homoserine Lactone Quorum-Sensing Signals Is Wide- Spread in Gram-Negative Methylobacterium J. Microbiol. Biotechnol. (2007), 17(2), 226–233 Production of Acyl-Homoserine Lactone Quorum-Sensing Signals is Wide- Spread in Gram-Negative Methylobacterium POONGUZHALI, SELVARAJ, MUNUSAMY MADHAIYAN, AND TONGMIN SA* Department of Agricultural Chemistry, Chungbuk National University, Cheongju, Chungbuk 361-763, Korea Received: August 2, 2006 Accepted: October 2, 2006 Abstract Members of Methylobacterium, referred as pink- knowledge on the Methylobacterium-plant interactions pigmented facultative methylotrophic bacteria, are frequently over the past two decades suggested interesting novel associated with terrestrial and aquatic plants, tending to form interactions between PPFMs and plants. Beneficial plant- aggregates on the phyllosphere. We report here that the production growth promoting bacteria interact with plants through of autoinducer molecules involved in the cell-to-cell signaling direct and indirect mechanisms. Direct mechanisms for the process, which is known as quorum sensing, is common among most part entail either providing the bacterial compounds Methylobacterium species. Several strains of Methylobacterium that promote plant growth or facilitating the uptake of were tested for their ability to produce N-acyl-homoserine nutrients; for example, production of phytohormones [9] lactone (AHL) signal molecules using different indicators. and siderophores [13]. The indirect effects occur through Most strains of Methylobacterium tested could elicit a suppression of one or more phytopathogenic microorganisms positive response in Agrobacterium tumefaciens harboring through biocontrol [20] or induction of plant defense lacZ fused to a gene that is regulated by autoinduction. The enzymes [14]. Beneficial effects of plant-Methylobacterium synthesis of these compounds was cell-density dependent, and associations have been suggested to be due to production the maximal activity was reached during the late exponential of phytohormones [22] and enzymes such as 1- to stationary phases. The bacterial extracts were separated by aminocyclopropane-1-carboxylate (ACC) deaminase [15] thin-layer chromatography and bioassayed with A. tumefaciens that promote plant growth directly or indirectly, fixation of NT1 (traR, tra::lacZ749). They revealed the production of nitrogen [32], and systemic resistance induced against various patterns of the signal molecules, which are strain pathogens [16]. Since methylotrophic bacteria tend to form dependent. At least two signal molecules could be detected in aggregates on the aerial parts of plants [31], the phenomenon most of the strains tested, and comparison of their relative of quorum sensing (QS), which affects the multicellular mobilities suggested that they are homologs of N-octanoyl-DL- behavior of bacteria in a community, gains importance. homoserine lactone (C8-HSL) and N-decanoyl-DL-homoserine Quorum sensing is a mechanism involved in cell density- lactone (C10-HSL). dependent bacterial communication that regulates the Key words: Quorum sensing, Methylobacterium, N-acyl- expression of specialized gene sets via secretion of homoserine lactone, thin-layer chromatography specific low-molecular weight signal molecules in a given environment. At a threshold concentration, these signal molecules act as co-inducers to regulate transcription of target genes, consequently triggering specific behavioral Bacteria of the genus Methylobacterium (PPFMs, pink- responses in a bacterial population that presumably benefit pigmented facultative methylotrophic bacteria) are strictly the bacteria in the particular habitat [2, 21]. Most but not aerobic, Gram-negative rods of α-Proteobacteria, capable all of the quorum-sensing systems discovered involves N- of growth on C1 compounds [12]. They are ubiquitous in acylated homoserine lactones (AHLs) as autoinducers. nature and frequently associated with terrestrial and aquatic AHLs consist of a homoserine lactone moiety linked to an plants, colonizing roots and leaf surfaces and potentially acyl side chain of variable length and substitution at the dominating the phyllosphere bacterial population [4]. The third carbon position that provide them with signal specificity. Much is known about the QS in a variety of *Corresponding author Phone: 82-43-261-2561; Fax: 82-43-271-5921; heterotrophic proteobacteria; however, AHL production by E-mail: [email protected] methylotrophic bacteria has not yet been conclusively QUORUM SENSING IN METHYLOBACTERIUM 227 documented to date. A recent study revealed the presence strains were routinely grown in ammonium mineral salts of two QS systems in M. extorquens AM1, with production (AMS) medium [35]. Chromobacterium violaceum CV026 of a novel long-chained C14:2 (N-tetradecenoyl) AHL [17] and C. violaceum ATCC12472 [18] were grown on Luria molecule [24]. broth (LB) (Difco Laboratories, Detroit, Michigan, U.S.A.) The objectives of this study were to survey the at 30oC without any drugs. Agrobacterium tumefaciens Methylobacterium strains for the presence of AHL quorum strains were grown on AB minimal media with 0.2% signals and, if present, to characterize these molecules by mannitol (ABM) [3] at 28oC. Pseudomonas putida F117 thin-layer chromatography (TLC) coupled to bioassays. (pRK-C12) [30] was grown on Luria Bertanii medium We further studied two Methylobacterium strains that had with 4 g of NaCl instead of 10 g of NaCl (MLB). The been proved to be plant-growth promoting, to study the following concentrations of antibiotics were used: gentamycin, production pattern of AHLs. Attempts were also made to 20 µg/ml; kanamycin, 50 µg/ml; spectinomycin, 50 µg/ml; confirm the presence of AHLs in the extracts through high- tetracycline, 4.5 µg/ml. X-Gal (5-bromo-4-chloro-3-indolyl- performance liquid chromatography (HPLC). β-D-galactopyranoside, BioShop Canada Inc., Burlington, ON, L7L4Y8) was supplemented in the medium for A. tumefaciens indicator bioassays. N-3-hexanoyl-DL-homoserine MATERIALS AND METHODS lactone (C6-HSL), N-(3-oxo-hexanoyl)-DL-homoserine lactone (3-oxo-C6-HSL), N-heptanoyl-DL-homoserine lactone (C7- Bacterial Strains and Culture Conditions HSL), N-octanoyl-DL-homoserine lactone (C8-HSL), and Methylobacterium strains CBMB20 (AY683045), CBMB110 N-decanoyl-DL-homoserine lactone (C10-HSL), N-dodecanoyl- (AY683046), CBMB120 (AY683047), CBMB130 (AY683048) DL-homoserine lactone (C12-HSL), and N-tetradecanoyl- tested for AHL production were isolated from rice and DL-homoserine lactone (C14-HSL) were purchased from found to possess plant-growth promoting characteristics Fluka and Sigma (Sigma-Aldrich Co., St. Louis, MO, [28]. Strains from different species of Methylobacterium, U.S.A.). screened for AHL production, along with their sources are listed in Table 1. Most strains were obtained from Deutsche Diffusion Bioassays Sammlung von Mikroorganismen und Zellkulturen GmbH One ml of overnight culture grown in ABM (A. tumefaciens (DSMZ), Germany. Few strains from the Korean Agriculture NT1, traR, tra::lacZ749 [25]) or LB (C. violaceum) was Collection Centre (KACC) and the Korean Collection for inoculated to 50 ml of the same medium and grown for Type Cultures (KCTC) were included. Methylobacterium 24 h at 30oC with shaking (120 rpm). The culture was then Table 1. List of Methylobacterium strains used for testing AHL production and their sources. Accession No. from DSMZ/ Genus and species/strain Source Reference KCTC, KACC collections Methylobacterium aquaticum DSM 16371T Drinking water Gallego et al. [8] Methylobacterium dichloromethanicum DSM 6343T Soil Doronina et al. [7] Methylobacterium extorquens DSM 1337T Soil Bousfield and Green [1] Methylobacterium fujisawaense KACC10744T Rhizoplane/M. sativa Green et al. [11] Methylobacterium hispanicum DSM 16372T Drinking water Gallego et al. [8] Methylobacterium lusitanum KCTC 12964T Sewage Doronina et al. [6] Methylobacterium mesophilicum DSM 1708T Phylloplane/L. perenne Green and Bousfield [10] Methylobacterium organophilum DSM 760T Sediment Patt et al. [23] Methylobacterium radiotolerans DSM 1819T Rice grains Green and Bousfield [10] Methylobacterium rhodesianum DSM 5687T Chlorinated water Green et al. [11] Methylobacterium rhodinum DSM 2163T Alnus rhizosphere Green and Bousfield [10] Methylobacterium suomiense KCTC 12963T Forest soil Doronina et al. [6] Methylobacterium thiocyanatum DSM 11490T A. aflatunense/soil Wood et al. [37] Methylobacterium zatmanii DSM 5688T Chlorinated water Green et al. [11] Methylobacterium sp. CBMB110 AY683046 Rice/leaf This study Methylobacterium sp. CBMB120 AY683047 Rhizosphere soil/rice This study Methylobacterium sp. CBMB130 AY683048 Rhizosphere soil/rice This study Methylobacterium sp. CBMB20 AY683045 Rice/stem This study TType strains collected from DSMZ, KCTC, or KACC collections. DSMZ, Deutsche Sammlung von Mikroorganismen und Zellkulturen GmbH, Germany; KACC, Korean Agriculture Collection Centre; KCTC, Korean Collection for Type Cultures. GenBank accession numbers for 16S ribosomal DNA sequences. 228 POONGUZHALI et al. poured to 100 ml of molten ABM with X-Gal (60 µg/ml) AHL standards including C6-HSL, C8-HSL, and C10-HSL. for A. tumefaciens NT1 (1.12% agar) or molten LB for C. Fractions were collected and assayed for AHLs, using violaceum (0.8% agar) at 46oC and immediately poured diffusion assay with A. tumefaciens NT1, as described over the surface of a 1.8% agar plate of the same medium. above, and fluorescence assay with P. putida F117 (pRK- Fifty µl of supernatant was loaded into wells (6 mm) C12) [30]. The fluorescence activity for
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