Antibiotic production by bacterial biocontrol agents

Interest in biological control of plant pathogens has been stimulated in recent years by trends in agriculture towards greater sustainability and public concern about the use of hazardous pesticides. There is now unequivocal evidence that antibiotics play a key role in the suppression of various soilborne plant pathogens by antagonistic microorganisms. The significance of antibiotics in biocontrol, and more generally in microbial interactions, often has been questioned because of the indirect nature of the supporting evidence and the perceived constraints to antibiotic production in rhizosphere environments. Reporter gene systems and bio-analytical techniques have clearly demonstrated that antibiotics are produced in the spermosphere and rhizosphere of a variety of host plants. Several abiotic factors such as oxygen, temperature, specific carbon and nitrogen sources, and microelements have been identified to influence antibiotic production by bacteria biocontrol agents. Among the biotic factors that may play a determinative role in antibiotic production are the plant host, the pathogen, the indigenous microflora, and the cell density of the producing strain. This review presents recent advances in our understanding of antibiotic production by bacterial biocontrol agents and their role in microbial interactions.

[1]  T. Mew,et al.  Isolation and identification of antifungal metabolites produced by rice-associated antagonistic Pseudomonas spp. , 1995 .

[2]  J. Parke,et al.  Postinfection Biological Control of Oomycete Pathogens of Pea by Burkholderia cepacia AMMDR1. , 2001, Phytopathology.

[3]  S. Lam,et al.  Four genes from Pseudomonas fluorescens that encode the biosynthesis of pyrrolnitrin , 1997, Applied and environmental microbiology.

[4]  J. Fels,et al.  Secondary Metabolite- and Endochitinase-Dependent Antagonism toward Plant-Pathogenic Microfungi of Pseudomonas fluorescens Isolates from Sugar Beet Rhizosphere , 1998, Applied and Environmental Microbiology.

[5]  R. Fani,et al.  Frequency and Biodiversity of 2,4-Diacetylphloroglucinol-Producing Bacteria Isolated from the Maize Rhizosphere at Different Stages of Plant Growth , 2000, Applied and Environmental Microbiology.

[6]  D. Weller,et al.  Effect of Population Density of Pseudomonas fluorescens on Production of 2,4-Diacetylphloroglucinol in the Rhizosphere of Wheat. , 1999, Phytopathology.

[7]  M. Schell,et al.  Characterization of Genes Involved in Biosynthesis of a Novel Antibiotic from Burkholderia cepacia BC11 and Their Role in Biological Control of Rhizoctonia solani , 1998, Applied and Environmental Microbiology.

[8]  S. Sarrocco,et al.  Characterization of a free-living maize-rhizosphere population of Burkholderia cepacia: effect of seed treatment on disease suppression and growth promotion of maize , 1998 .

[9]  N. Stuurman,et al.  Simultaneous imaging of Pseudomonas fluorescens WCS365 populations expressing three different autofluorescent proteins in the rhizosphere: new perspectives for studying microbial communities. , 2000, Molecular plant-microbe interactions : MPMI.

[10]  M. Bailey,et al.  Identification of conserved traits in fluorescent pseudomonads with antifungal activity. , 2000, Environmental microbiology.

[11]  T. Paulitz,et al.  A Novel Antifungal Furanone from Pseudomonas aureofaciens, a Biocontrol Agent of Fungal Plant Pathogens , 2000, Journal of Chemical Ecology.

[12]  C. Keel,et al.  Influence of enhanced antibiotic production in pseudomonas fluorescens strain cha0 on its disease suppressive capacity , 1992 .

[13]  K. Qing.  Systemic resistance induced by rhizosphere bacteria , 2001 .

[14]  D. Weller.  Colonization of wheat roots by a fluorescent pseudomonad suppressive to take-all. , 1983 .

[15]  C. R. Howell.  Control of rhizoctonia solani on cotton seedlings with Pseudomonas fluorescens and with an antibiotic produced by the bacterium. , 1979 .

[16]  F. O'Gara,et al.  Exploitation of gene(s) involved in 2,4-diacetylphloroglucinol biosynthesis to confer a new biocontrol capability to a Pseudomonas strain , 1992, Applied and Environmental Microbiology.

[17]  Cook Rj.  Making greater use of introduced microorganisms for biological control of plant pathogens. , 1993 .

[18]  F. O'Gara,et al.  Role of 2,4-Diacetylphloroglucinol in the Interactions of the Biocontrol Pseudomonad Strain F113 with the Potato Cyst Nematode Globodera rostochiensis , 1997, Applied and environmental microbiology.

[19]  C. Keel,et al.  Conservation of the 2,4-diacetylphloroglucinol biosynthesis locus among fluorescent Pseudomonas strains from diverse geographic locations , 1996, Applied and environmental microbiology.

[20]  J. Handelsman,et al.  Biocontrol of Soilborne Plant Pathogens. , 1996, The Plant cell.

[21]  R. Fani,et al.  Biodiversity of a Burkholderia cepacia population isolated from the maize rhizosphere at different plant growth stages , 1997, Applied and environmental microbiology.

[22]  D. Gottlieb,et al.  The production and role of antibiotics in soil. , 1976, The Journal of antibiotics.

[23]  J. Handelsman,et al.  Biological activities of two fungistatic antibiotics produced by Bacillus cereus UW85 , 1994, Applied and environmental microbiology.

[24]  A. Brandis,et al.  Pyrrolnitrin Production by an Enterobacter agglomerans Strain with a Broad Spectrum of Antagonistic Activity Towards Fungal and Bacterial Phytopathogens , 1996, Current Microbiology.

[25]  M. Bailey,et al.  Chromosomal insertion of phenazine-1-carboxylic acid biosynthetic pathway enhances efficacy of damping-off disease control by Pseudomonas fluorescens. , 2000, Molecular plant-microbe interactions : MPMI.

[26]  C. Dorschel.  The role of particle-beam LC-MS in separation development , 1997 .

[27]  B. Ownley.  Influence of in situ and in vitro pH on suppression of Gaeumannomyces graminis var. tritici by Pseudomonas fluorescens 2-79. , 1992 .

[28]  A. Boronin,et al.  A Seven-Gene Locus for Synthesis of Phenazine-1-Carboxylic Acid by Pseudomonas fluorescens2-79 , 1998, Journal of bacteriology.

[29]  J. Handelsman,et al.  Zwittermicin A-producing strains of Bacillus cereus from diverse soils , 1994, Applied and environmental microbiology.

[30]  Y. Hashidoko,et al.  Possible Role of Xanthobaccins Produced byStenotrophomonas sp. Strain SB-K88 in Suppression of Sugar Beet Damping-Off Disease , 1999, Applied and Environmental Microbiology.

[31]  L. Thomashow,et al.  Identification and Characterization of a Gene Cluster for Synthesis of the Polyketide Antibiotic 2,4-Diacetylphloroglucinol from Pseudomonas fluorescens Q2-87 , 1999, Journal of bacteriology.

[32]  F. Gong,et al.  Molecular analysis of genes encoding phenazine biosynthesis in the biological control bacterium. Pseudomonas aureofaciens 30-84. , 1995, FEMS microbiology letters.

[33]  G. Berg,et al.  Strains of the genus Serratia as beneficial rhizobacteria of oilseed rape with antifungal properties. , 1996, Microbiological research.

[34]  P. Bakker,et al.  Biocontrol by Phenazine-1-carboxamide-Producing Pseudomonas chlororaphis PCL1391 of Tomato Root Rot Caused by Fusarium oxysporum f. sp. radicis-lycopersici , 1998 .

[35]  H. Hoitink,et al.  BIOCONTROL WITHIN THE CONTEXT OF SOIL MICROBIAL COMMUNITIES: A Substrate-Dependent Phenomenon. , 1999, Annual review of phytopathology.

[36]  L. Thomashow,et al.  Current Concepts in the Use of Introduced Bacteria for Biological Disease Control: Mechanisms and Antifungal Metabolites , 1996 .

[37]  P. Williams,et al.  Plants genetically modified to produce N-acylhomoserine lactones communicate with bacteria , 1999, Nature Biotechnology.

[38]  T. Paulitz,et al.  Novel butyrolactones with antifungal activity produced by Pseudomonas aureofaciens strain 63-28. , 1997, The Journal of antibiotics.

[39]  D. Weller,et al.  Genetic analysis of the antifungal activity of a soilborne Pseudomonas aureofaciens strain , 1991, Applied and environmental microbiology.

[40]  J. Handelsman,et al.  Production of kanosamine by Bacillus cereus UW85. Appl Environ Microbiol , 1996 .

[41]  J. Loper,et al.  Characterization of a Genomic Region Required for Production of the Antibiotic Pyoluteorin by the Biological Control Agent Pseudomonas fluorescens Pf-5 , 1995, Applied and environmental microbiology.

[42]  N. Koedam,et al.  Involvement of phenazines and anthranilate in the antagonism of Pseudomonas aeruginosa PNA1 and Tn5 derivatives toward Fusarium spp. and Pythium spp. , 1998 .

[43]  S. Lindow.  The use of reporter genes in the study of microbial ecology , 1995 .

[44]  B. Binder,et al.  Flow cytometric detection of specific gene expression in prokaryotic cells using in situ RT-PCR. , 2000, FEMS microbiology letters.

[45]  M. Moran,et al.  In situ PCR for visualization of microscale distribution of specific genes and gene products in prokaryotic communities , 1995, Applied and environmental microbiology.

[46]  J. D. Elsas,et al.  Methods for the introduction of bacteria into soil: A review , 1990, Biology and Fertility of Soils.

[47]  J. Handelsman,et al.  Genotypic and phenotypic analysis of zwittermicin A-producing strains of Bacillus cereus. , 1996, Microbiology.

[48]  J. Vickers,et al.  The ecology of antibiotic production , 1986, Microbial Ecology.

[49]  M. Zala,et al.  Biocontrol of soil-borne fungal plant diseases by 2,4-diacetylphloroglucinol-producing fluorescent pseudomonads with different restriction profiles of amplified 16S rDNA , 1998, European Journal of Plant Pathology.

[50]  J. Handelsman,et al.  Synergy Between Zwittermicin A and Bacillus thuringiensis subsp. kurstaki Against Gypsy Moth (Lepidoptera: Lymantriidae) , 2000 .

[51]  M. Jackson,et al.  Nutritional factors regulating growth and accumulation of phenazine 1-carboxylic acid by Pseudomonas fluorescens 2-79 , 1992, Applied Microbiology and Biotechnology.

[52]  F. O'Gara,et al.  Isolation of 2,4-Diacetylphloroglucinol from a Fluorescent Pseudomonad and Investigation of Physiological Parameters Influencing Its Production , 1992, Applied and environmental microbiology.

[53]  B. Duffy,et al.  Environmental Factors Modulating Antibiotic and Siderophore Biosynthesis by Pseudomonas fluorescensBiocontrol Strains , 1999, Applied and Environmental Microbiology.

[54]  J Loper,et al.  POLYKETIDE PRODUCTION BY PLANT-ASSOCIATED PSEUDOMONADS. , 1999, Annual review of phytopathology.

[55]  J. Ziegle,et al.  Molecular cloning of genetic determinants for inhibition of fungal growth by a fluorescent pseudomonad , 1986, Journal of bacteriology.

[56]  Kevin P. Smith,et al.  Genetic basis in plants for interactions with disease-suppressive bacteria. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[57]  D. Hill,et al.  Natural products with antifungal activity from Pseudomonas biocontrol bacteria , 2000 .

[58]  J. T. Smith,et al.  Inhibition of Septoria tritici and other phytopathogenic fungi and bacteria by Pseudomonas fluorescens and its antibiotics , 1992 .

[59]  C. Keel,et al.  Suppression of root diseases by Pseudomonas fluorescens CHA0 - importance of the bacterial seconday metabolite 2,4-diacetylphloroglucinol , 1992 .

[60]  M. Schroth,et al.  Cloning of a phenazine biosynthetic locus of Pseudomonas aureofaciens PGS12 and analysis of its expression in vitro with the ice nucleation reporter gene , 1994, Applied and environmental microbiology.

[61]  S. Gould,et al.  Characterization of the Pyoluteorin Biosynthetic Gene Cluster of Pseudomonas fluorescens Pf-5 , 1999, Journal of bacteriology.

[62]  J. D. Elsas,et al.  Molecular Microbial Ecology Manual , 2013, Springer Netherlands.

[63]  K. van Pée,et al.  Conservation of the pyrrolnitrin biosynthetic gene cluster among six pyrrolnitrin-producing strains. , 1999, FEMS microbiology letters.

[64]  D. Weller,et al.  Exploiting Genotypic Diversity of 2,4-Diacetylphloroglucinol-Producing Pseudomonas spp.: Characterization of Superior Root-Colonizing P. fluorescensStrain Q8r1-96 , 2001, Applied and Environmental Microbiology.

[65]  S. Hill,et al.  Global regulation of expression of antifungal factors by a Pseudomonas fluorescens biological control strain. , 1994, Molecular plant-microbe interactions : MPMI.

[66]  M. Pettinari,et al.  A PCR-based method for the screening of bacterial strains with antifungal activity in suppressive soybean rhizosphere , 2001 .

[67]  D. Weller,et al.  Natural plant protection by 2,4-diacetylphloroglucinol-producing Pseudomonas spp. in take-all decline soils , 1998 .

[68]  P. Slininger,et al.  Pyrrolnitrin Production by Biological Control Agent Pseudomonas cepacia B37w in Culture and in Colonized Wounds of Potatoes , 1994, Applied and environmental microbiology.

[69]  J. Whipps,et al.  Microbial interactions and biocontrol in the rhizosphere. , 2001, Journal of experimental botany.

[70]  G. Berg.  Diversity of antifungal and plant‐associated Serratia plymuthica strains , 2000, Journal of applied microbiology.

[71]  L. Thomashow,et al.  Role of a phenazine antibiotic from Pseudomonas fluorescens in biological control of Gaeumannomyces graminis var. tritici , 1988, Journal of bacteriology.

[72]  J. Handelsman,et al.  Target Range of Zwittermicin A, an Aminopolyol Antibiotic from Bacillus cereus , 1998, Current Microbiology.

[73]  J. Handelsman,et al.  Production of kanosamine by Bacillus cereus UW85 , 1996, Applied and environmental microbiology.

[74]  David M. Weller,et al.  Biological control of soilborne plant pathogens in the rhizosphere with bacteria , 1988 .

[75]  T. Chin-A-Woeng,et al.  Description of the Colonization of a Gnotobiotic Tomato Rhizosphere by Pseudomonas fluorescens Biocontrol Strain WCS365, Using Scanning Electron Microscopy , 1997 .

[76]  J. Whipps.  Developments in the Biological Control of Soil-borne Plant Pathogens , 1997 .

[77]  L. Thomashow,et al.  Cloning and heterologous expression of the phenazine biosynthetic locus from Pseudomonas aureofaciens 30-84. , 1992, Molecular plant-microbe interactions : MPMI.

[78]  J. Handelsman,et al.  Zwittermicin A biosynthetic cluster. , 1999, Gene.

[79]  A. Kerr.  Biological control of crown gall through production of Agrocin 84. , 1980 .

[80]  L. Thomashow,et al.  phzO, a Gene for Biosynthesis of 2-Hydroxylated Phenazine Compounds in Pseudomonas aureofaciens 30-84 , 2001, Journal of bacteriology.

[81]  D. Haas,et al.  Pseudomonads as antagonists of plant pathogens in the rhizosphere: role of the antibiotic 2,4-diacetylphloroglucinol in the suppression of black root rot of tobacco. , 1990 .

[82]  J. Parke,et al.  Diversity of the Burkholderia cepacia complex and implications for risk assessment of biological control strains. , 2001, Annual review of phytopathology.

[83]  D. Crawford,et al.  Antibiotics and enzymes produced by the biocontrol agent Streptomyces violaceusniger YCED-9 , 1998, Journal of Industrial Microbiology and Biotechnology.

[84]  L. Thomashow,et al.  Frequency of Antibiotic-Producing Pseudomonas spp. in Natural Environments , 1997, Applied and environmental microbiology.

[85]  Winkelmann,et al.  Pyrrolnitrin from Burkholderia cepacia: antibiotic activity against fungi and novel activities against streptomycetes , 1998, Journal of applied microbiology.

[86]  A. Sarniguet,et al.  The sigma factor sigma s affects antibiotic production and biological control activity of Pseudomonas fluorescens Pf-5. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[87]  D. Fravel,et al.  Role of Antibiosis in the Biocontrol of Plant Diseases , 1988 .

[88]  S. Beer,et al.  Pantoea agglomerans Strain EH318 Produces Two Antibiotics That Inhibit Erwinia amylovoraIn Vitro , 2001, Applied and Environmental Microbiology.

[89]  S. Kalloger,et al.  Genotypic and Phenotypic Diversity of phlD-ContainingPseudomonas Strains Isolated from the Rhizosphere of Wheat , 2000, Applied and Environmental Microbiology.

[90]  R. Cook.  Making greater use of introduced microorganisms for biological control of plant pathogens. , 1993, Annual review of phytopathology.

[91]  F. Gong,et al.  N-acyl-homoserine lactone-mediated regulation of phenazine gene expression by Pseudomonas aureofaciens 30-84 in the wheat rhizosphere , 1997, Journal of bacteriology.

[92]  K. Kang,et al.  Isolation and identification of antifungal N-butylbenzenesulphonamide produced by Pseudomonas sp. AB2. , 2000, The Journal of antibiotics.