Bases of biocontrol: Sequence predicts synthesis and mode of action of agrocin 84, the Trojan Horse antibiotic that controls crown gall

Kim, Jung Gun; Park, Byoung Keun; Kim, Sung Uk; Choi, Doil; Nahm, Baek Hie; Moon, Jae Sun; Reader, John S.; Farrand, Stephen K.; Hwang, Ingyu

doi:10.1073/pnas.0602965103

Cited by 80 publications

(77 citation statements)

References 38 publications

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“…Database comparisons revealed that the backbone of pAMI2 described above is conserved in pAgK84 of Agrobacterium radiobacter K84, a plasmid responsible for the production of the antiagrobacterial compound agrocin 84 (21). Plasmids pAMI2 and pAgK84 carry related replication, partitioning, and transfer systems in synteny, which strongly suggests that they originate from a common ancestor replicon (data not shown).…”

Section: Resultsmentioning

confidence: 98%

Plasmid pAMI2 of Paracoccus aminophilus JCM 7686 Carries N , N -Dimethylformamide Degradation-Related Genes Whose Expression Is Activated by a LuxR Family Regulator

Dziewit

Dmowski

Baj

et al. 2010

Appl Environ Microbiol

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N,N-Dimethylformamide (DMF), a toxic solvent used in the chemical industry, is frequently present in industrial wastes. Plasmid pAMI2 (18.6 kb) of Paracoccus aminophilus JCM 7686 carries genetic information which is crucial for methylotrophic growth of this bacterium, using DMF as the sole source of carbon and energy. Besides a conserved backbone related to pAgK84 of Agrobacterium radiobacter K84, pAMI2 carries a three-gene cluster coding for the protein DmfR, which has sequence similarities to members of the LuxR family of transcription regulators, and two subunits (DmfA1 and DmfA2) of N,N-dimethylformamidase, an enzyme of high substrate specificity that catalyzes the first step in the degradation of DMF. Genetic analysis revealed that these genes, which are all placed in the same orientation, constitute an inducible operon whose expression is activated in the presence of DMF by the positive transcription regulator DmfR. This operon was used to construct a strain able to degrade DMF at high concentrations that might be used in the biotreatment of DMF-containing industrial wastewaters. To our knowledge, this is the first study to provide insights into the genetic organization and regulation as well as the dissemination in bacteria of genes involved in the enzymatic breakdown of DMF.

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Section: Resultsmentioning

confidence: 98%

Plasmid pAMI2 of Paracoccus aminophilus JCM 7686 Carries N , N -Dimethylformamide Degradation-Related Genes Whose Expression Is Activated by a LuxR Family Regulator

Dziewit

Dmowski

Baj

et al. 2010

Appl Environ Microbiol

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“…Many plant-associated bacteria make bacteriocins, such as agrocin, produced by Agrobacterium radiobacter strain K84. This bacteriocin excludes the crown gall pathogen A. tumefaciens from the infection court so effectively that A. radiobacter is widely used for biocontrol (54).…”

Section: Figmentioning

confidence: 99%

Tropical Strains of Ralstonia solanacearum Outcompete Race 3 Biovar 2 Strains at Lowland Tropical Temperatures

Huerta

Milling

Allen

2015

Appl Environ Microbiol

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Bacterial wilt, caused by members of the heterogenous Ralstonia solanacearum species complex, is an economically important vascular disease affecting many crops. Human activity has widely disseminated R. solanacearum strains, increasing their global agricultural impact. However, tropical highland race 3 biovar 2 (R3bv2) strains do not cause disease in tropical lowlands, even though they are virulent at warm temperatures. We tested the hypothesis that differences in temperature adaptation and competitive fitness explain the uneven geographic distribution of R. solanacearum strains. Using three phylogenetically and ecologically distinct strains, we measured competitive fitness at two temperatures following paired-strain inoculations of their shared host, tomato. Lowland tropical strain GMI1000 was only weakly virulent on tomato under temperate conditions (24°C for day and 19°C for night [24/19°C]), but highland tropical R3bv2 strain UW551 and U.S. warm temperate strain K60 were highly virulent at both 24/19°C and 28°C. Strain K60 was significantly more competitive than both GMI1000 and UW551 in tomato rhizospheres and stems at 28°C, and GMI1000 also outcompeted UW551 at 28°C. The results were reversed at cooler temperatures, at which highland strain UW551 generally outcompeted GMI1000 and K60 in planta. The superior competitive index of UW551 at 24/19°C suggests that adaptation to cool temperatures could explain why only R3bv2 strains threaten highland agriculture. Strains K60 and GMI1000 each produced different bacteriocins that inhibited growth of UW551 in culture. Such interstrain inhibition could explain why R3bv2 strains do not cause disease in tropical lowlands. Ralstonia solanacearum, which causes bacterial wilt disease of many crops, is found on six continents, and its hosts include plants in over 50 dicot and monocot families. The pathogen forms a heterogenous species complex that contains thousands of distinct strains (1, 2). No single strain can attack all known hosts, but most members of the species complex can wilt tomato. The best way to manage bacterial wilt is by planting resistant crop varieties, but the high variability of the pathogen complicates breeding efforts because wilt resistance is often strain specific (3, 4). Sequencing over 20 diverse strains revealed that R. solanacearum has a fluid genome with evidence of extensive horizontal gene transfer (5-7). However, the specific mechanisms by which this pathogen has adapted to diverse environments and hosts are unknown. For example, most strains of R. solanacearum are tropical or subtropical, but one highly adapted group, known historically and for regulatory purposes as race 3 biovar 2 (R3bv2), causes economically important wilt of both potato and tomato in cool highland tropics (8).R. solanacearum strains fall into four genetically distinct phylotypes that correspond to their geographic origin: phylotypes I (Asia), II (the Americas), III (Africa), and IV (Indonesia) (1) However, because of human activity, multiple phylotypes are now commonly...

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“…The first five structural genes, accABCDE, code for an ABC-type transport system that takes up agrocinopines as well as a unique antibiotic called agrocin 84 (27,34). Agrocin 84 is produced by A. radiobacter strain K84, which is antagonistic to A. tumefaciens strain C58 competing for agrocinopines that are produced by plants transformed by A. tumefaciens strain C58 (19,36,47,48,56,64,67). The last two genes, accF and accG, code for agrocinopine phosphodiesterase and arabinose phosphate phosphatase, respectively (34, 73).…”

mentioning

confidence: 99%

Opine-BasedAgrobacteriumCompetitiveness: Dual Expression Control of the Agrocinopine Catabolism (acc) Operon by Agrocinopines and Phosphate Levels

Kim

Myung

et al. 2008

J Bacteriol

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Agrobacterium tumefaciens strain C58 can transform plant cells to produce and secrete the sugar-phosphate conjugate opines agrocinopines A and B. The bacterium then moves in response to the opines and utilizes them as exclusive sources of carbon, energy, and phosphate via the functions encoded by the acc operon. These privileged opine-involved activities contribute to the formation of agrobacterial niches in the environment. We found that the expression of the acc operon is induced by agrocinopines and also by limitation of phosphate. The main promoter is present in front of the first gene, accR, which codes for a repressor. This operon structure enables efficient repression when opine levels are low. The promoter contains two putative operators, one overlapping the ؊10 sequence and the other in the further upstream from it; two partly overlapped putative pho boxes between the two operators; and two consecutive transcription start sites. DNA fragments containing either of the operators bound purified repressor AccR in the absence of agrocinopines but not in the presence of the opines, demonstrating the on-off switch of the promoter. Induction of the acc operon can occur under low-phosphate conditions in the absence of agrocinopines and further increases when the opines also are present. Such opine-phosphate dual regulatory system of the operon may ensure maximum utilization of agrocinopines when available and thereby increase the chances of agrobacterial survival in the highly competitive environment with limited general food sources.During agrobacterial infection of susceptible plants, a copy of the T region in a tumor-inducing plasmid (Ti plasmid), called the T-DNA, is transferred from the bacterium to the plant where it becomes integrated into the chromosome (10)(11)(12)25). Expression of the genes on the integrated T-DNA results in the tumorous phenotype and also the production of unusual low-molecular-weight carbon compounds that belong to a large group of plant tumor-specific metabolites collectively called opines (15,20,58,66).Crown gall tumors induced by the classic nopaline-type Agrobacterium tumefaciens strain C58 synthesize and secrete two families of tumor metabolites: agrocinopines A and B and nopaline (20,43). The genes responsible for the biosynthesis of agrocinopines and of nopaline are carried on the T region of pTiC58, harbored by the strain C58 (7,14,29). Strain C58 can catabolize nopaline and agrocinopines by using functions encoded by two different sets of genes located on the nontransferred region of the Ti plasmid (6, 27, 34, 76). These loci, called acc (agrocinopine catabolism) and noc (nopaline catabolism), code for the transport and catabolism of, as well as chemotaxis to, their cognate opines (34,35,51,76).The process by which A. tumefaciens transforms plant cells to produce opines has been termed genetic colonization of the plant (60). The genetic colonization theory leads to the opine concept, proposed by Tempé et al. (68), which states that the opines are the chemical mediators of t...

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Bases of biocontrol: Sequence predicts synthesis and mode of action of agrocin 84, the Trojan Horse antibiotic that controls crown gall

Cited by 80 publications

References 38 publications

Plasmid pAMI2 of Paracoccus aminophilus JCM 7686 Carries N , N -Dimethylformamide Degradation-Related Genes Whose Expression Is Activated by a LuxR Family Regulator

Plasmid pAMI2 of Paracoccus aminophilus JCM 7686 Carries N , N -Dimethylformamide Degradation-Related Genes Whose Expression Is Activated by a LuxR Family Regulator

Tropical Strains of Ralstonia solanacearum Outcompete Race 3 Biovar 2 Strains at Lowland Tropical Temperatures

Opine-BasedAgrobacteriumCompetitiveness: Dual Expression Control of the Agrocinopine Catabolism (acc) Operon by Agrocinopines and Phosphate Levels

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