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Acyl Homoserine Lactone-Based Quorum Sensing in a Methanogenic Archaeon

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Acyl Homoserine Lactone-Based Quorum Sensing in a Methanogenic Archaeon The ISME Journal (2012) 6, 1336–1344 & 2012 International Society for Microbial Ecology All rights reserved 1751-7362/12 www.nature.com/ismej ORIGINAL ARTICLE Acyl homoserine lactone-based quorum sensing in a methanogenic archaeon Guishan Zhang1, Fan Zhang1, Gang Ding2, Jie Li1, Xiaopeng Guo1, Jinxing Zhu1, Liguang Zhou1, Shichun Cai1, Xiaoli Liu1, Yuanming Luo1, Guifeng Zhang3, Wenyuan Shi4 and Xiuzhu Dong1 1State Key Laboratory of Microbial Resources, Institute of Microbiology, Chinese Academy of Sciences, Beijing, PR China; 2Institute of Medicinal Plant Development, Chinese Academy of Medical Sciences and Peking Union Medical College, Beijing, PR China; 3State Key Laboratory of Biochemical Engineering, Institute of Process Engineering, Chinese Academy of Sciences, Beijing, PR China and 4Department of Microbiology, Immunology and Molecular Genetics, University of California, Los Angeles, CA, USA Acyl homoserine lactone (AHL)-based quorum sensing commonly refers to cell density-dependent regulatory mechanisms found in bacteria. However, beyond bacteria, this cell-to-cell communication mechanism is poorly understood. Here we show that a methanogenic archaeon, Methanosaeta harundinacea 6Ac, encodes an active quorum sensing system that is used to regulate cell assembly and carbon metabolic flux. The methanogen 6Ac showed a cell density-dependent physiology transition, which was related to the AHL present in the spent culture and the filI gene-encoded AHL synthase. Through extensive chemical analyses, a new class of carboxylated AHLs synthesized by FilI protein was identified. These carboxylated AHLs facilitated the transition from a short cell to filamentous growth, with an altered carbon metabolic flux that favoured the conversion of acetate to methane and a reduced yield in cellular biomass. The transcriptomes of the filaments and the short cell forms differed with gene expression profiles consistent with the physiology. In the filaments, genes encoding the initial enzymes in the methanogenesis pathway were upregulated, whereas those for cellular carbon assimilation were downregulated. A luxI–luxR ortholog filI–filR was present in the genome of strain 6Ac. The carboxylated AHLs were also detected in other methanogen cultures and putative filI orthologs were identified in other methanogenic genomes as well. This discovery of AHL-based quorum sensing systems in methanogenic archaea implies that quorum sensing mechanisms are universal among prokaryotes. The ISME Journal (2012) 6, 1336–1344; doi:10.1038/ismej.2011.203; published online 12 January 2012 Subject Category: microbe–microbe and microbe–host interactions Keywords: carboxylated acyl homoserine lactones; filI-encoded AHL synthase; methanogenic archaea; physiology transition; quorum sensing Introduction system, whereas Gram-positive bacteria use small peptides as autoinducers. Despite the ubiquity of Quorum sensing is a well-characterized gene-regu- quorum sensing systems in bacteria, quorum sen- latory mechanism that coordinates diverse social sing has yet to be conclusively identified in archaea, behaviours in bacteria, such as biofilm formation, except that a bacterial biosensor was reported to antibiotic resistance, production of luminescence, detect potential quorum sensing signals from a exotoxins and exopolysaccharides, and uptake of halophilic archaeon (Paggi et al., 2003) and genome extracellular DNA (Hastings and Greenberg, 1999; analyses suggest that LuxS-based AI-2 signalling Waters and Bassler, 2005). In this process, bacteria may be present (Sun et al., 2004). communicate through secreted signal molecules or We previously isolated an obligate aceticlastic autoinducers, which are involved in gene regula- methanogenic archaeon, Methanosaeta harundina- tion. The Gram-negative bacteria use acyl homo- cea 6Ac, from the up-flow anaerobic sludge bed serine lactones (AHLs) as a quorum sensing signal to granules in an anaerobic digester (Ma et al., 2006). achieve regulation through the luxI–luxR homolog Intriguingly, this methanogen shows a cell density- dependent cell assembly (as described below), Correspondence: X Dong, State Key Laboratory of Microbial making it a good model system for the study of Resources, Institute of Microbiology, Chinese Academy of quorum sensing behaviour in archaea. In the present Sciences, No.1 West Beichen Road, Beijing 100101, PR China. E-mail: [email protected] study, a bacterial luxI–luxR-like circuit was obs- Received 26 April 2011; revised 21 November 2011; accepted 28 erved in M. harundinacea 6Ac and a luxI homolog November 2011; published online 12 January 2012 called the filI gene was shown to encode AHL Quorum sensing in a methanogenic archaeon G Zhang et al 1337 synthase. This archaeal enzyme synthesized a group Rosseta (DE3) strain. The FilI protein was purified by of carboxylated AHL with 10–14 carbon atoms in the HisTrap HP and Q ion exchange column chromato- acyl chain. Furthermore, these carboxyl-AHLs acted graphy (GE Healthcare, Piscataway, NJ, USA). as the quorum sensing signal in regulating the physiology of M. harundinacea 6Ac. Therefore this methanogenic archaeon uses a quorum sensing Enzymatic synthesis of AHLs by FilI system similar to that used by Gram-negative The principle of in vitro enzymatic synthesis of bacteria. AHLs was described elsewhere (More et al., 1996; Val and Cronan, 1998). Briefly, S-adenylmethionine was the substrate for the homoserine lactone moiety Materials and methods and the cell-free extract of strain 6Ac was the source Methanogen strain and growth conditions of acyl-carrier proteins (ACPs), according to the M. harundinacea 6Ac was maintained in our presence of a b-ketoacyl-acyl carrier protein laboratory and routinely cultured in a pre-reduced synthase gene fabH (Mhar_2367) in the genome, although no ACP homologue is found in the basal medium containing 50 mM sodium acetate, yeast extract (0.05%, w/v) and peptone (0.05%, w/v) genome. Cells in mid-log phase were collected by as described previously (Doddema and Vogels, 1978; centrifugation, resuspended in TEDG buffer (10 mM Ma et al., 2006). To promote the formation of Tris-HCl (pH 8.0), 0.1 mM EDTA, 0.1 mM dithiothrei- filaments, the acetate in growing cultures was tol, 5% glycerol), and disrupted by ultrasonication for 30 min on ice. The cell lysate was centrifuged at replenished up to three times with 50 mM sodium acetate. 20 000 g for 1 h and the supernatant of about 5 mg protein per ml was used for ACPs. FilI synthesis reactions (200 ml) were performed in microfuge tubes N-acyl-homoserine lactone bioassay at 37 1C for 30 min. The reaction mixture contained Agrobacterium tumefaciens NTL4, which carries the 10 mM Tris-HCl (pH 7.4), 330 mM NaCl, 15% plasmid pZLR4, was used as an N-acyl-homoserine glycerol, 0.7 mM dithiothreitol, 2 mM EDTA, 25 mM lactone reporter. Plasmid pZLR4 contains a MgSO4, 0.1 mM FeSO4, and 0.15 mM S-adenyl- traG::lacZ fusion and traR (Steindler and Venturi, methionine and 60 ml cell-free extract of strain 2007). The plate assay for detection of AHLs was 6Ac, unless otherwise indicated. The reaction performed as described previously (Hwang et al., was initiated by adding 6 mg per ml of His6-FilI 1994). Briefly, AB agar containing 0.2–0.5% glucose and stopped by adding three volumes of ethyl and 40 mgmlÀ1 X-gal was poured into Petri dishes, acetate. The ethyl acetate phase was collected and then half of the plate was overlaid with 0.7% agar dried in a rotary vacuum evaporator at 30 1C. containing the reporter strain NTL4, whereas an- The residue was re-suspended in methanol for other half was overlaid with only 0.7% agar as a purification of AHLs. blank. After the overlay solidified, 5 ml of the test liquid was spotted onto to the soft agar on both halves of the plate. The plates were incubated at Purification of FilI-synthesized AHLs 28 1C for 12–48 h. Formation of blue spots indicated AHLs synthesized by FilI were purified using the presence of AHLs in the test sample. AHLs in the an Agilent ZORBAX Extend-C18 Column spent culture were quantified according to the (4.6 Â 250 mm, 5 mm particle size) on Agilent’s 1100 method of Cha et al. (1998). Series HPLC, and monitored with a Finnigan SpectraSYSTEM UV6000LP PDA Detector and LCQ Deca XPplus ion-trap mass spectrometer (Thermo- Cloning of filI gene, and expression and purification Finnigan, San Jose, CA, USA) (Ortori et al., 2007). of FilI protein The purification parameters were as follows: The genomic DNA of M. harundinacea 6Ac was column temperature 15 1C; mobile phase-A, water extracted as described previously (Zhou et al., 1996) with 0.01% trifluoroacetic acid; mobile phase-B, and was used as template for PCR amplification of acetonitrile with 0.01% frifluoroacetic acid; flow ORF00438 (GenBank no. HQ188282) (filI). The rate, 0.8 ml minÀ1; gradient profile, linear increase of primer pair shown in Supplementary Table S3 was phase-B from 30 to 90% over 5–65 min. The column used for PCR amplification of the filI gene. PCR was re-equilibrated for a total of 15 min prior to 50 ml amplification was performed using Pfu DNA poly- loading. The three AHL compounds were collected merase (Promega, Madison, WI, USA) for 30 cycles, in the elute fractions with a retention time of with each cycle consisting of denaturation at 95 1C 25–35 min. for 45 s, annealing at 59 1C for 1 min and elongation at 72 1C for 5 min. The PCR product was purified using the 3S Spin Agarose Gel DNA Purification Mass spectral determination of AHLs kit (Shanghai Biocolor Bioscience and Technology Electrospray ionization mass spectra were recorded Company, Shanghai, China) and cloned into the in the positive ionization mode using a LCQ Deca pET28a vector for expression in the Escherichia coli XPplus ion-trap mass spectrometer (Thermo-Finnigan) The ISME Journal Quorum sensing in a methanogenic archaeon G Zhang et al 1338 (Cataldi et al., 2009). Samples in 50% methanol express 2.0 software, Primer Premier 5.0 and Oligo 6.0.
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