characteristics of the lrha subfamily of transcriptional

E---40-2--10-166-07180.mdiActa Biochim Biophys Sin (2008) | Volume 40 | Issue 2 | Page 166
Sinorhizobium meliloti lrhA subfamily genesActa Biochim Biophys Sin (2008): 166-173 | © 2008 Institute of Biochemistry and Cell Biology, SIBS, CAS | All Rights Reserved 1672-9145 http://www.abbs.info; www.blackwellpublishing.com/abbs | DOI: 10.1111/j.1745-7270.2008.00378.x
Characteristics of the LrhA subfamily of transcriptional regulators from Sinorhizobium meliloti
Mingsheng Qi1,2#, Li Luo1,2#, Haiping Cheng3, Jiabi Zhu1, and Guanqiao Yu1* 1 Laboratory of Molecular Genetics, Shanghai Institute of Plant Physiology and Ecology, Shanghai Institute for Biological Sciences,
Chinese Academy of Sciences, Shanghai 200032, China 2 Graduate School of the Chinese Academy of Science s, Beijing 100049, China 3 Biological Sciences Department, Lehman College, City University of New York, New York 10468, USA
Received: June 20, 2007 Accepted: October 29, 2007 This work was supported by the grants from National Key Program for Basic Research of China (No. 2001CB108901) # These authors contributed equally to this work *Corresponding author: Tel, 86-21-54924165; Fax, 86-21-54924015; E-mail, [email protected]
In our previous work, we identified 94 putative genes encod- ing LysR-type transcriptional regulators from Sinorhizobium meliloti. All of these putative lysR genes were mutagenized using plasmid insertions to determine their phenotypes. Six LysR-type regulators, encoded by mutants SMa1979, SMb20715, SMc00820, SMc04163, SMc03975, and SMc04315, showed similar amino acid sequences (30%) and shared the conserved DNA-binding domain with LrhA, HexA, or DgdR. Phenotype analysis of these gene mutants indicated that the regulators control the swimming behaviors of the bacteria, production of quorum-sensing signals, and secretion of extracellular proteins. These characteristics are very similar to those of LrhA, HexA, and DgdR. Thus, we refer to this group as the LrhA subfamily. Sequence analysis showed that a great number of homologous genes of the LrhA subfamily were distributed in the α, β, and γ subdi- visions of proteobacteria, and a few in actinobacteria. These findings could provide new clues to the roles of the LysR gene family.
Keywords LrhA subfamily; LysR-type transcriptional regulator; Sinorhizobium meliloti
The LysR family of regulators, evolved from distant ancestors, are broadly distributed in prokaryotic genera. The structure and function of the LysR family of transcriptional regulators are conserved to some extent. They are typically approximately 300 amino acids long with an
N-terminal DNA-binding domain participating in the recognition of target promoter, and a C-terminal domain for sensing signal molecules [1]. They function as transcriptional activators or repressors. Typically they regulate genes with promoters different from their own. The promoters of the target genes often have a conserved sequence and typically at least one TN11A motif [1]. The conserved and divergently oriented promoters of target genes to lysR regulatory genes can facilitate the quick recognition of these promoters for us.
One of the LysR-type regulator genes, lrhA from Escherichia coli, is located upstream of the nuoA-N (NADH:quinone oxidoreductase) locus [2]. LrhA mainly functions in controlling the transcription of flagella, motility, and chemotaxis genes by regulating the expression of the flhDC regulon, the master regulator of flagella- and motility-related genes [3]. The LrhA protein is highly homologous to HexA from Erwinia carotovora (64% identity) and PecT from Erwinia chrysanthemi (61% identity). In some phytopathogenic bacteria, HexA and PecT act as motility repressors and virulence factors, such as exoenzymes required for lytic reactions [4,5]. Overexpression of the Erw. carotovora hexA gene in the opportunistic human patho- gen Serratia also represses multiple virulence determinants [5]. In hexA mutants of Erw. carotovora, expression of flagella genes (fliA and fliC) is increased, thereby result- ing in hypermotility [5]. In the same organism, HexA also regulates the production of the regulatory RNA rsmB (a homolog of the E. coli csrB), the quorum-sensing phero- mone N-(3-oxohexanoyl)-L-homoserine lactone, and the stationary phase sigma factor RpoS [6].
In our previous work [7], 94 putative LysR family genes were mutagenized by the insertion of suicide plasmids. Phenotype determination of these mutants indicated that mutation of six genes among them impaired the motility of
Acta Biochim Biophys Sin (2008) | Volume 40 | Issue 2 | Page 167
Sinorhizobium meliloti lrhA subfamily genes
the strains in rich medium. The products encoded by these six genes are highly homologous with LrhA and HexA; they belong to the same clade, as revealed by the phylog- eny analysis of 90 putative LysR family genes. Referring to HexA, several other experiments were also carried out, such as homoserine lactone assay and quantification of extracellular protein. Three mutants, Sm326, Sm341, and Sm360 excreted less N-acyl homoserine lactone (AHL) than the wild-type Rm1021, whereas the other three mutants had no difference from the wild type. Only Sm326 secreted more extracellular proteins than the wild type. These findings suggested that these six LysR-type regulators have sequences and functions similar to those of LrhA and HexA. In particular, product encoded by SMa1979 showed functions in regulating cell motility, AHL production, and extracellular protein secretion similar to those of Erw. carotovora HexA. We refer to this group as the LrhA subfamily.
Therefore, homologs of LrhA genes from sequenced bacterial genomes were collected to find significantly different distributions in those bacteria by analyzing their genomic sequences.
Materials and Methods
Bacterial strains and medium The bacterial strains used in this work are listed in Table
1. Luria-Bertani (LB) medium was used for the growth of E. coli. The ZMGS (10 g/L mannitol, 1 g/L glutamic acid, 1 g/L K2PO4, 1 mg/ml MnCl2, 0.1 mg/ml H3BO3, 0.1 mg/ ml ZnSO4·7H2O, 0.1 mg/ml CoCl2·6H2O, 0.1 mg/ml CuSO4·5H2O, 10 mg/ml FeCl3, 1 mg/ml biotin, and 1 mg/ ml thiamine) and LB media used for Sinorhizobium meliloti were supplemented with 2.5 mM MgSO4 and 2.5 mM CaCl2 (LB/MC). Agar (1.5%) was used as the solid media. Antibiotics were used at the following concentrations: kanamycin, 25 µg/ml; ampicillin, 100 µg/ml; neomycin, 200 µg/ml; streptomycin, 500 µg/ml; tetracycline, 10 µg/ ml; spectinomycin, 100 µg/ml; and gentamicin, 50 µg/ml.
Motility test Cell motility was examined using both microscopy and medium for swimming as described previously by Wei and Bauer [13]. Briefly, bacterial strains were inoculated onto LB/MC and ZMGS soft agar media (0.3%) and incubated for 4 d to determine their colony size. Photographs were taken using a Nikon Coolpix 4500 digital camera (Nikon, Tokyo, Japan).
AHL bioassay AHL assays were carried out as reported by Marketon and González [14] with some modifications. Briefly, 150 µl supernatant of bacteria culture was mixed with 30 µl indicator strain Agrobacterium tumefaciens NTL4 (pZLR4)
Table 1 Strains of bacteria used in this work
Bacterial strains or plasmids Relevant characteristics Reference or source
Sinorhizobium meliloti Rm1021 Strr, derivative of SU47 [8] Sm326 SMa1979::pK19mob2HMB [7] Sm341 SMb20715::pK19mob2HMB [7] Sm360 SMc00820::pK19mob2HMB [7] Sm379 SMc04163::pK19mob2HMB [7] Sm382 SMc03975::pK19mob2HMB [7] Sm383 SMc04315::pK19mob2HMB [7] Agrobacterium tumefaciens NTL4 (pZLR4) Derivative of NT1 carrying a traG::lacZ reporter fusion Agrr, Gmr [9,10] Escherichia coli DH5α SupE44lacU169(80lacZ15)hsdR17recA1endA1 Laboratory stock MT616 Pro-82thi-1endA1supE44−,Cmr, carrying pRK600 [11] Plasmids pAtC58 Cryptic plasmid of A. tumefaciens [10] pTiC58accR Derivative of pTiC58 with a deletion in the accR gene, Trac [12]
Agrr, agrocin 84 resistance; AHL, N-acyl-homoserine lactone; Cmr, chloramphenicol resistance; Gmr, gentamicin resistance; Strr, streptomycin resistance; Tcs, tetracycline sensitive; Trac, transfer constitutive.
[9]. NTL4 (pAtC58) and NTL4 (pAtC58, pTiC58accR) were used as the negative and positive controls, respectively [10,15]. The relative amount of AHL of those bacteria was determined by measuring the β-galactosidase ac- tivity of the indicator strain after 3 h. The β-galactosidase assays were carried out as described by Miller [16]. Spec- trophotometer 7200 (Tianmei Scientific Equipment Cooperation, Shanghai, China) was used in this work.
Total extracellular protein assays Quantitative spectrophotometric assays were carried out to assess the total extracellular proteins produced by the wild type and mutants of the LrhA subfamily regulator when OD600 nm is 0.2, 2.0, and 5.0, using the Coomassie Brilliant Blue G-250 method described by Bradford [14].
Multiple sequence alignment The putative LysR-type regulator sequences were sourced from the website http://bioinfo.genopole-toulouse.prd.fr/ annotation/iANT/bacteria/rhime/. ClustalW (http://www. ebi.ac.uk/Tools/clustalw2/index.html) was used to align multiple sequences and construct the evolutionary tree, and all default parameters were selected.
Results
Six LysR family regulators belong to an LrhA subfamily The deduced amino acid sequences of 94 LysR family regulators from S. meliloti Rm1021 were sourced from the website http://bioinfo.genopole-toulouse.prd.fr/annotation/iANT/bacteria/rhime/. Those sequences were input into the EBI ClustalW server to construct a phylogenetic tree. Six members of the LysR family, that is, products encoded by mutants SMa1979, SMb20715, SMc00820, SMc04163, SMc03975, and SMc04315, were located on the same clade of the evolutionary tree (data not shown). Each of these regulators showed approximately 30% ho- mology with E. coli LrhA, Erw. carotovora HexA, or Pseu- domonas putida DgdR by BlastP analysis (http://www. ncbi.nlm.nih.gov/blast/Blast.cgi?PAGE=Proteins& PROGRAM=blastp&BLAST_PROGRAMS=blastp&PAGE_ TYPE=BlastSearch&SHOW_DEFAULTS=on). Results of multiple sequence alignments indicated that these six regulators were highly homologous to LrhA, HexA, and DgdR, especially in the DNA-binding domains, although the C- terminal domains were quite variable in length (Fig. 1). These analyses revealed that these genes could be classi- fied into an LrhA subfamily of the LysR family of regulator genes.
Effect of the mutations of LrhA subfamily regulators on motility The motility of six LysR-type regulator mutants was determined on the LB/MC or ZMGS swimming agar plates. All mutants migrated more slowly than the wild-type strain (Rm1021) on LB/MC agar (Fig. 2). After 4 d of culture, the diameters of their colonies were 86.6%±0.5% to 93.5%±0.5% of that of Rm1021. On the ZMGS agar plates, Sm341 had a slightly higher mobility than Rm1021 (data not shown), whereas the other five mutants swam more slowly than the wild type. This result indicated that mutation of these five genes impairs their swimming mobility.
Effect of the mutations of LrhA subfamily regulators on AHL accumulation The strain A. tumefaciens NTL4 (pZLR4) was used as an indicator to measure the transcriptional level of traG (as traG-lacZ fusion is controlled by AHL-like signals) [15], to assess the relative amount of AHL in rhizobia culture. NTL4 (pAtC58) and NTL4 (pAtC58, pTiC58accR) were used as the negative and positive controls, respectively. The mutants Sm379, Sm382, and Sm383 showed similar AHL concentrations to that with the wild type, although Sm382 had a 4-fold increase at OD600 nm=1.45. Much lower levels of AHL were found in the cultures of Sm326, Sm341, and Sm360 (Fig. 3). These results suggested that Sm326, Sm341, and Sm360 were defective in AHL production even in complete medium.
Effect of the mutations of LrhA subfamily regulators on extracellular protein production Quantitative spectrophotometric assays were carried out to assess the total extracellular proteins produced by the mutants of LrhA subfamily regulator at three growth phases. The level of total extracellular proteins produced by SMa1979 mutant strain Sm326 became 1-fold, 4-fold, and 2-fold higher than Rm1021 at OD600 nm=0.2, 2.0, and 5.0, respectively, but the results on other mutants showed no such significant difference (Fig. 4). The extracellular protein secretion was observed at much higher levels in SMa1979 mutant strain Sm326 compared with a wild- type strain control at an early stationary phase. These results are very similar to those of hexA mutation in Erw. carotovora ssp. carotovora [6].
SMa1979 mutation (Sm326) resulted in impairment in motility, defects in AHL production, and increased secretion of extracellular protein, as in the Erw. carotovora hexA mutant; and SMb20715, SMc00820, and SMc03975 had
Fig. 1 Multiple sequence alignment of LrhA homologs in Sinorhizobium meliloti Amino acid residues identical throughout the LrhA subfamily are shaded in black, similar residues are shaded in gray. Gaps are marked with “–” and subfamily names are indicated at the beginning of each line. LrhA was from Escherichia coli, HexA was from Erwinia carotovora, and DgdR was from Pseudomonas putida.
Fig. 2 Motility of LrhA homologous gene mutants from Sinorhizobium meliloti (A) A sample of 3 µl resuspended culture of wild-type Rm1021 and mutants of the six LrhA homologs was spotted onto LB/MC (Luria-Bertani medium supplemented with 2.5 mM MgSO4 and 2.5 mM CaCl2) soft agar media (0.35%) and incubated at 30 ºC for 4 d. (B) Relative diameters of each mutant colony compared with that of the wild type.
Fig. 3 Level of N-acyl homoserine lactone (AHL) signal in Sinorhizobium meliloti LrhA homolog mutants The levels of AHL signal in cultures of different s trains were measured at OD600 nm=0.36, 1.45, and 2.00. NTL4 (pAtC58) and NTL4 (pAtC58, pTiC58accR) were applied as the negative and positive controls, respectively.
similar functions to E. coli lrhA.
LrhA subfamily genes in other bacteria As many bacterial genomes have been sequenced and published, it is possible to search for more LrhA subfamily genes and conveniently analyze their origin and evolution.
The deduced amino acid sequence of E. coli LrhA was input into the National Center for Biotechnology Information’s Blast/genome server (http://www.ncbi.nlm. nih.gov/sutils/genom_table.cgi) to search for homologous genes in other bacterial genomes (e<0.0001, Score>80,
Fig. 4 Extracellular protein produced by Sinorhizobium meliloti LrhA mutants Total extracellular protein produced by the wild type (Rm1021) and mutants of the LrhA subfamily regulator were measured at OD600 nm=0.2, 2.0, and 5.0.
Dec, 2004). The LrhA subfamily homologous genes were found in bacteria, not in archaea. Furthermore, 140 genes were found in proteobacteria, but only six genes in actinobacteria. Among the 140 genes found in proteobacteria, 39 genes were distributed in the α subgroup, 65 genes in the β subgroup, and 36 genes in the γ subgroup (Fig. 5), but none were found in either the δ or the ε subgroups. In the α subgroup, there are LrhA homologs in Rhizobium, such as the 6 genes in S. meliloti Rm1021, 10 genes in Mezorhizobium loti MAFF303099, and 7 genes in A. tumefaciens C58 [Fig. 5(A)]. A large number of LrhA genes were found in Burkholderia, for example, 17 genes in
Burkholderia cepacia R18194 [Fig. 5(B)]. However, there was only one homolog found in most species of the γ subgroup; only Pseudomonas aeruginosa PAO1 contained five members [Fig. 5(C)]. These results suggest that the distribution of the LrhA subfamily is significantly different in different bacterial families.
Discussion
The known number of LysR family genes has increased
with the publication of bacterial genome sequences. Many bacteriologists are interested in the functions of these regulators in nature. Schell [1] wrote a review in 1993, but a lot of new genes have since been found to have novel roles in metabolism, symbiosis, and bacterial swimming, such as LrhA, HexA, and PecT [4].
With an increase in the number of genome sequences, sequence analysis is a preferred tool for analyzing functions of target genes. A new subfamily belonging to the LysR family was suggested because the amino acid se-
Fig. 5 Distribution of LrhA subfamily genes in proteobacteria LrhA homologs in other bacterial genomes, sourced from the National Center for Biotechnology Information’s BLAST/genome server (http://www.ncbi.nlm.nih.gov/sutils/genom_table.cgi) (e<0.0001, Score>80, Dec 2004). (A) Number of LrhA homologs in the α subgroup. (B) Number of LrhA homologs in the β subgroup. (C) Number of LrhA homologs in the γ subgroup. At, Agrobacterium tumefaciens; Av, Alcanivorax borkumensis SK2; Bb, Bordetella bronchiseptica; Bc1, Burkholderia cenocepacia; Bc2, Burkholderia cepacia; Bf, Burkholderia phymatum; Bj, Bradyrhizobium japonicum; Bm, Brucella melitensis; Bma, Burkholderia mallei; Bpa, Bordetella parapertussis; Bpe, Bordetella pertussis; Bps, Burkholderia pseudomallei; Bs, Brucella suis; Cv, Chromobacterium violaceum; Ec, Escherichia coli 101-1; Eco1, Escherichia coli 536; Eco2, Escherichia coli B171; Eco3, Escherichia coli K12; Il, Idiomarina loihiensis; Lp1, Legionella pneumophila str. Corby; Lp2, Legionella pneumophila str. Lens; Lp3, Legionella pneumophila str. Paris; Ml, Mesorhizobium loti; Msp, Mesorhizobium sp. BNC1; Na, Novosphingobium aromaticivorans; Pa1, Psychrobacter arcticus 273-4; Pa2, Pseudoalteromonas atlantica; Pf, Psychromonas ingrahamii 37; Pl, Photorhabdus luminescens; Pp, Psychrobacter sp. PRwf-1; Psy, Psychrobacter cryohalolentis K5; Psy2, Psychromonas sp. CNPT3; Re, Ralstonia eutropha; Rm, Ralstonia metallidurans; Rp, Rhodopseudomonas palustris; Rs, Rickettsia sibirica; Rsc, Ralstonia solanacearum; Se1, Salmonella enterica ssp. enterica serovar Choleraesuis str. SC-B67; Se2, Salmonella enterica ssp. enterica serovar Newport str. SL254; Sm, Sinorhizobium meliloti; Sp, Silicibacter pomeroyi; Spsp, Sphingomonas sp. SKA58; St, Salmonella typhimurium; Vp, Vibrionales bacterium SWAT-3; Vv, Vibrio vulnificus; Yp1, Yersinia pestis Antiqua; Yp2, Yersinia pestis Pestoides F .
quences shared similar identities with those of E. coli LrhA and Erw. carotovora HexA. The sequences were also located on one clade of the evolutionary tree, providing many clues to identify the functions of these genes. The results of genome sequence analyses suggest that this subfamily is distributed in some bacterial species, but not all.
The motility of all mutants of the S. meliloti LrhA subfamily, except Sm341, was impaired on both complete and minimum media. It is interesting to note that the motility of the mutant SMb20715 was different on these two media. It swam slower than the wild-type on the LB/ MC medium [7], but quicker on the ZMGS medium. One assumption is that lower nutrient supply might promote the chemotaxis of rhizobia.
Furthermore, three gene mutants had fewer AHL signals, whereas the mutant SMc03975 had a 4-fold increase. The effects of these mutations will be determined in further studies. Sm326, an SMa1979 mutant, had significantly more extracellular protein than the wild type. It is appar- ent that this mutant had phenotypes similar to those of E. coli lrhA and Erwinia hexA.
It is interesting to study how these genes can affect the motility of rhizobia and the relationship between the production of AHL and motility. It has been reported that, in many bacteria, swarming motility is quorum-sensing controlled [19]. It was shown that AHL-dependent synthesis of the biosurfactants is required for swarming motility [20− 23], although AHL-deficient mutants of Pseudomonas syringae pv. syringae B728a had high motility [24]. In S. meliloti, swarming of the mutant 8530 strain could be dependent on SinI- and/or ExpR-mediated quorum sensing [25]. It might be hypothesized that these genes affect the motility of rhizobia by affecting the production of AHL, but this needs to be proven in future works. Why did the mutant of SMa1979, Sm326, produce more extracellular protein? The characteristics of these unknown extracellular proteins, and promoters of regulatory genes and target genes will be investigated in our laboratory.
Acknowledgements
We thank Dr. Stephen Farrand (Department of Microbiology, University of Illinois at Urbana-Champaign) for providing A. tumefaciens NTL4 (pZLR4), NTL4 (pAtC58), and NTL4 (pAtC58, pTiC58accR). We thank Prof. Tianduo Wang (retired) for revising the manuscript.
References
1 Schell MA. Molecular biology of the LysR family of transcriptional
regulators. Annu Rev Microbiol 1993, 47: 597−626 2 Bongaerts J, Zoske S, Weidner U, Unden G. Transcriptional regula-
tion of the proton-translocating NADH dehydrogenase genes (nuoA- N) of Escherichia coli by electron acceptors, electron donors and gene regulators. Mol Microbiol 1995, 16: 521−534
3 Pratt LA, Silhavy TJ. The response regulator SprE controls the stability of RpoS. Proc Natl Acad Sci USA 1996, 93: 2488−2492
4 Surgey N, Robert-Baudouy J , Condemine G. The Erwinia chrysanthemi pecT gene regulates pectinase gene expression. J Bacteriol 1996, 178: 1593−1599
5 Harris SJ, Shih YL, Bentley SD, Salmond GP. The hexA gene of Erwinia carotovora encodes a LysR homologue and regulates motility and the expression of multiple virulence determinants. Mol Microbiol 1998, 28: 705−717
6 Mukherjee A, Cui Y, Ma W, Liu Y, Chatterjee AK. hexA of Erwinia carotovora ssp. carotovora strain Ecc71 negatively regulates production of RpoS and rsmB RNA, a global regulator of extracellular proteins, plant virulence and the quorum-sensing signal, N-(3- oxohexanoyl)-L-homoserine lactone. Environ Microbiol 2000, 2: 203−215
7 Luo L, Yao SY, Becker A, Ruberg S, Yu GQ, Zhu JB, Cheng HP. Two new Sinorhizobium meliloti LysR-type transcriptional regulators required for nodulation. J Bacteriol 2005, 187: 4562−4572
8 Meade HM, Long SR, Ruvkun GB, Brown SE, Ausubel FM. Physical and genetic characterization of symbiotic and auxotrophic mutants of Rhizobium meliloti induced by transposon mutagenesis. J Bacteriol 1982, 149: 114−122
9 Buch C, Sigh J, Nielsen J, Larsen JL, Gram L. Production of acylated homoserine lactones by different serotypes of Vibrio anguillarum both in culture and during infection of rainbow trout. Syst Appl Microbiol 2003, 26: 338−349
1 0 Luo ZQ, Clemente TE, Farrand SK. Construction of a derivative of Agrobacterium tumefaciens C58 that does not mutate to tetracycline resistance. Mol Plant Microbe Interact 2001, 14: 98−103
1 1 Finan TM, Kunkel B, De Vos GF, Signer ER. Second symbiotic megaplasmid in Rhizobium meliloti carrying exopolysaccharide and thiamine synthesis genes. J Bacteriol 1986, 167: 66−72
1 2 Luo ZQ, Farrand SK. The Agrobacterium tumefaciens rnd homolog is required for TraR-mediated quorum-dependent activation of Ti plasmid tra gene expression. J Bacteriol 2001, 183: 3919−3930
1 3 Wei X, Bauer WD. Tn5-induced and spontaneous switching of Sinorhizobium meliloti to faster-swarming behavior. Appl Environ Microbiol 1999, 65: 1228−1235
1 4 Marketon MM, González JE. Identification of two quorum-sensing systems in Sinorhizobium meliloti. J Bacteriol 2002, 184: 3466−3475
1 5 Beck von Bodman S, McCutchan JE, Farrand SK. Characterization of the conjugal transfer functions of Agrobacterium tumefaciens Ti plasmid pTiC58. J Bacteriol 1989, 171: 5281−5289
1 6 Miller J. Experiments in molecular genetics. New York: Cold Spring Harbor Laboratory Press, 1972
1 7 Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein- dye binding. Anal Biochem 1976, 72: 248−254
1 8 Piper KR, Farrand SK. Quorum sensing but not autoinduction of Ti plasmid conjugal transfer requires control by the opine regulon and the antiactivator TraM. J Bacteriol 2000, 182: 1080−1088
1 9 Daniels R, Vanderleyden J, Michiels J. Quorum sensing and swarming migration in bacteria. FEMS Microbiol Rev 2004, 28: 261−289
2 0 Lindum PW, Anthoni U, Christophersen C, Eberl L, Molin S, Givskov M. N-Acyl-L-homoserine lactone autoinducers control production
of an extracellular lipopeptide biosurfactant required for swarming motility of Serratia liquefaciens MG1. J Bacteriol 1998, 180: 6384− 6388
2 1 Ochsner UA, Reiser J . Autoinducer-mediated regulation of rhamnolipid biosurfactant synthesis in Pseudomonas aeruginosa. Proc Natl Acad Sci USA 1995, 92: 6424−6428
2 2 Huber B, Riedel K, Hentzer M, Heydorn A, Gotschlich A, Givskov M, Molin S et al. The cep quorum-sensing system of Burkholderia cepacia H111 controls biofilm formation and swarming motility. Microbiology 2001, 147: 2517−2528
2 3 Malott RJ, Baldwin A, Mahenthiralingam E, Sokol PA. Character- ization of the cciIR quorum-sensing system in Burkholderia cenocepacia. Infect Immun 2005, 73: 4982−4992
2 4 Quiñones B, Dulla G, Lindow SE. Quorum sensing regulates exopolysaccha ride production, motil ity , and vi ru lence in Pseudomonas syringae. Mol Plant Microbe Interact 2005, 18: 682−693

characteristics of the lrha subfamily of transcriptional

Documents