Home LiteratureArticle Details
PMID: 12571047 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S. Research Support, U.S. Gov't, P.H.S.

Use of a promoter trap to identify Bacillus cereus genes regulated by tomato seed exudate and a rhizosphere resident, Pseudomonas aureofaciens.

Applied and environmental microbiology ·Vol. 69 ·No. 2 ·2003-02-00 ·Pages 1197-205

Dunn AK, Klimowicz AK, Handelsman J

Abstract

The goal of this study was to identify genes in Bacillus cereus, a bacterium commonly associated with plant seeds and roots, that are affected by compounds originating from a host plant, tomato, or another rhizosphere resident, Pseudomonas aureofaciens. We constructed a B. cereus chromosomal DNA library in a promoter-trap plasmid, pAD123, which contains a promoterless version of the green fluorescent protein (GFP) gene, gfpmut3a. The library was screened by using fluorescence-activated cell sorting for clones showing a change in GFP expression in response to either tomato seed exudate or culture supernatant of P. aureofaciens strain 30-84. We identified two clones carrying genes that were induced by the presence of tomato seed exudate and nine clones carrying genes that were repressed by P. aureofaciens culture supernatant. A clone chosen for further study contained an open reading frame, designated lipA, that encodes a deduced protein with a lipoprotein signal peptide sequence similar to lipoproteins in B. subtilis. Expression of gusA under control of the lipA promoter increased twofold when cells were exposed to tomato seed exudate and in a concentration-dependent manner when exposed to a mixture of amino acids. When the wild type and a 10-fold excess of a lipA mutant were applied together to tomato seeds, 2 days after planting, the wild type displayed medium-dependent culturability, whereas the lipA mutant was unaffected. This study demonstrates the power of a promoter trap to identify genes in a gram-positive bacterium that are regulated by the biotic environment and resulted in the discovery of lipA, a plant-regulated gene in B. cereus.

MeSH Terms
Bacillus cereus/genetics,growth & development Bacterial Proteins/genetics,metabolism Gene Expression Regulation, Bacterial Lipoproteins Lycopersicon esculentum/microbiology Membrane Proteins Molecular Sequence Data Plant Roots/microbiology Promoter Regions, Genetic Pseudomonas/growth & development Seeds/microbiology Sequence Analysis, DNA Transcription, Genetic
Chemicals
Bacterial Proteins LipA protein, Bacteria Lipoproteins Membrane Proteins prsA protein, bacteria
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Dunn Anne K
Department of Bacteriology, University of Wisconsin-Madison, Madison, Wisconsin 53706, USA.
Klimowicz Amy K
Handelsman Jo
References (40)
40 references, click to expand
  1. Genetic basis in plants for interactions with disease-suppressive bacteria.
    Proc Natl Acad Sci U S A. 1999 Apr 27;96(9):4786-90 PMID: 10220371
  2. Bacillus subtilis PrsA is required in vivo as an extracytoplasmic chaperone for secretion of active enzymes synthesized either with or without pro-sequences.
    Mol Microbiol. 1993 May;8(5):957-66 PMID: 8102773
  3. Studies on transformation of Escherichia coli with plasmids.
    J Mol Biol. 1983 Jun 5;166(4):557-80 PMID: 6345791
  4. A plant flavone, luteolin, induces expression of Rhizobium meliloti nodulation genes.
    Science. 1986 Aug 29;233(4767):977-80 PMID: 3738520
  5. Effect of canavanine from alfalfa seeds on the population biology of bacillus cereus
    Appl Environ Microbiol. 1998 Dec;64(12):4683-8 PMID: 9835549
  6. A new family of peptidyl-prolyl isomerases.
    Trends Biochem Sci. 1995 Jan;20(1):12-4 PMID: 7878731
  7. The PrsA lipoprotein is essential for protein secretion in Bacillus subtilis and sets a limit for high-level secretion.
    Mol Microbiol. 1993 May;8(4):727-37 PMID: 8332065
  8. Biological Control of Damping-Off of Alfalfa Seedlings with Bacillus cereus UW85.
    Appl Environ Microbiol. 1990 Mar;56(3):713-8 PMID: 16348145
  9. Identification of plant-induced genes of the bacterial pathogen Xanthomonas campestris pathovar campestris using a promoter-probe plasmid.
    EMBO J. 1987 Jan;6(1):23-8 PMID: 15981331
  10. Tomato seed and root exudate sugars: composition, utilization by Pseudomonas biocontrol strains and role in rhizosphere colonization.
    Environ Microbiol. 1999 Oct;1(5):439-46 PMID: 11207764
  11. Identification of plant-inducible genes in Erwinia chrysanthemi 3937.
    J Bacteriol. 1990 Mar;172(3):1569-75 PMID: 2155205
  12. Construction and characterization of a human bacterial artificial chromosome library.
    Genomics. 1996 Jun 1;34(2):213-8 PMID: 8661051
  13. beta-Glucuronidase (GUS) transposons for ecological and genetic studies of rhizobia and other gram-negative bacteria.
    Microbiology. 1995 Jul;141 ( Pt 7):1691-705 PMID: 7551037
  14. Pseudomonas aureofaciens nov. spec. and its pigments.
    J Bacteriol. 1956 Sep;72(3):406-11 PMID: 13366937
  15. Phylogeny of the main bacterial 16S rRNA sequences in Drentse A grassland soils (The Netherlands).
    Appl Environ Microbiol. 1998 Mar;64(3):871-9 PMID: 9501427
  16. Root Exudate-Induced Promoter Activity in Pseudomonas fluorescens Mutants in the Wheat Rhizosphere.
    Appl Environ Microbiol. 1995 Mar;61(3):890-8 PMID: 16534972
  17. Culture conditions that influence accumulation of zwittermicin A by Bacillus cereus UW85.
    Appl Microbiol Biotechnol. 1995 Aug-Sep;43(4):685-91 PMID: 7546606
  18. Nucleotide sequence of the tetracycline resistance gene of pBC16 from Bacillus cereus.
    Nucleic Acids Res. 1990 Mar 25;18(6):1635 PMID: 2109312
  19. Genotypic and phenotypic analysis of zwittermicin A-producing strains of Bacillus cereus.
    Microbiology. 1996 Dec;142 ( Pt 12):3425-36 PMID: 9004505
  20. Evidence for mutualism between a plant growing in a phosphate-limited desert environment and a mineral phosphate solubilizing (MPS) rhizobacterium.
    FEMS Microbiol Ecol. 1999 Dec 1;30(4):295-300 PMID: 10568838
  21. Two-way chemical signaling in Agrobacterium-plant interactions.
    Microbiol Rev. 1992 Mar;56(1):12-31 PMID: 1579105
  22. Role of a phenazine antibiotic from Pseudomonas fluorescens in biological control of Gaeumannomyces graminis var. tritici.
    J Bacteriol. 1988 Aug;170(8):3499-508 PMID: 2841289
  23. Fluorescence-based isolation of bacterial genes expressed within host cells.
    Science. 1997 Sep 26;277(5334):2007-11 PMID: 9302299
  24. Recombinant inbred lines for genetic mapping in tomato.
    Theor Appl Genet. 1995 Mar;90(3-4):542-8 PMID: 24173949
  25. Adaptation of Pseudomonas fluorescens to the plant rhizosphere.
    Environ Microbiol. 1999 Jun;1(3):243-57 PMID: 11207743
  26. Antibiotic-resistance cassettes for Bacillus subtilis.
    Gene. 1995 Dec 29;167(1-2):335-6 PMID: 8566804
  27. Assessment of bacterial pathogenesis by analysis of gene expression in the host.
    Annu Rev Genet. 2000;34:139-164 PMID: 11092824
  28. Gene cluster of Pseudomonas syringae pv. "phaseolicola" controls pathogenicity of bean plants and hypersensitivity of nonhost plants.
    J Bacteriol. 1986 Nov;168(2):512-22 PMID: 3023280
  29. Two-component transcriptional regulation of N-acyl-homoserine lactone production in Pseudomonas aureofaciens.
    Appl Environ Microbiol. 1999 Jun;65(6):2294-9 PMID: 10347004
  30. Zwittermicin A-producing strains of Bacillus cereus from diverse soils.
    Appl Environ Microbiol. 1994 Dec;60(12):4404-12 PMID: 7811080
  31. Influence of tomato genotype on growth of inoculated and indigenous bacteria in the spermosphere.
    Appl Environ Microbiol. 2001 Feb;67(2):514-20 PMID: 11157211
  32. Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mp18 and pUC19 vectors.
    Gene. 1985;33(1):103-19 PMID: 2985470
  33. In vivo expression technology strategies: valuable tools for biotechnology.
    Curr Opin Biotechnol. 2000 Oct;11(5):440-4 PMID: 11024360
  34. Modeling dose-response relationships in biological control: partitioning host responses to the pathogen and biocontrol agent.
    Phytopathology. 1997 Jul;87(7):720-9 PMID: 18945094
  35. The role of lipoprotein processing by signal peptidase II in the Gram-positive eubacterium bacillus subtilis. Signal peptidase II is required for the efficient secretion of alpha-amylase, a non-lipoprotein.
    J Biol Chem. 1999 Jan 15;274(3):1698-707 PMID: 9880550
  36. A vector for promoter trapping in Bacillus cereus.
    Gene. 1999 Jan 21;226(2):297-305 PMID: 9931504
  37. Toward functional genomics in bacteria: analysis of gene expression in Escherichia coli from a bacterial artificial chromosome library of Bacillus cereus.
    Proc Natl Acad Sci U S A. 1999 May 25;96(11):6451-5 PMID: 10339608
  38. Biological activities of two fungistatic antibiotics produced by Bacillus cereus UW85.
    Appl Environ Microbiol. 1994 Jun;60(6):2023-30 PMID: 8031096
  39. Genetic analysis of crown gall: fine structure map of the T-DNA by site-directed mutagenesis.
    Cell. 1981 Nov;27(1 Pt 2):143-53 PMID: 6276020
  40. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs.
    Nucleic Acids Res. 1997 Sep 1;25(17):3389-402 PMID: 9254694
Article Info
Journal
Applied and environmental microbiology
Abbr.
Appl Environ Microbiol
ISSN
0099-2240
Published
2003-02-00
Pages
1197-205
Language
English
Region
United States
NLM ID
7605801
PMCID
PMC143612
Subset
IM
Grants
NIGMS NIH HHS · T32 GM007215 · United States
NIGMS NIH HHS · T32 GM008349 · United States
NIGMS NIH HHS · 5 T32 GM07215 · United States
NIGMS NIH HHS · 5 T32 GM08349 · United States
Databases
GENBANK
AY169374, AY169375, AY169376, AY169377, AY169378, AY169379, AY169380, AY169381, AY169382, AY169383, AY169384
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com