Resistance to ultraviolet light in Pseudomonas syringae: sequence and functional analysis of the plasmid-encoded rulAB genes

Sundin, George W.; Kidambi, Saranga P.; Ullrich, Matthias S.; Bender, Carol L.

doi:10.1016/0378-1119(96)00273-9

Cited by 60 publications

(49 citation statements)

References 16 publications

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“…Various plasmids in Pseudomonas have been shown to express the UV mutagenesis phenotype, i.e., an increase in mutation frequency of up to 100-fold above spontaneous levels (35,36,40,56,60). We found that the transfer of TOL plasmid pWW0 into the plasmid-free strain P. putida PaW85 also resulted in an increased frequency of mutations if bacteria were irradiated with UV-C light.…”

Section: Resultsmentioning

confidence: 75%

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A DNA Polymerase V Homologue Encoded by TOL Plasmid pWW0 Confers Evolutionary Fitness on Pseudomonas putida under Conditions of Environmental Stress

et al. 2005

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Plasmids in conjunction with other mobile elements such as transposons are major players in the genetic adaptation of bacteria in response to changes in environment. Here we show that a large catabolic TOL plasmid, pWW0, from Pseudomonas putida carries genes (rulAB genes) encoding an error-prone DNA polymerase Pol V homologue which increase the survival of bacteria under conditions of accumulation of DNA damage. A study of population dynamics in stationary phase revealed that the presence of pWW0-derived rulAB genes in the bacterial genome allows the expression of a strong growth advantage in stationary phase (GASP) phenotype of P. putida. When rulAB-carrying cells from an 8-day-old culture were mixed with Pol V-negative cells from a 1-day-old culture, cells derived from the aged culture out-competed cells from the nonaged culture and overtook the whole culture. At the same time, bacteria from an aged culture lacking the rulAB genes were only partially able to out-compete cells from a fresh overnight culture of the parental P. putida strain. Thus, in addition to conferring resistance to DNA damage, the plasmid-encoded Pol V genes significantly increase the evolutionary fitness of bacteria during prolonged nutritional starvation of a P. putida population. The results of our study indicate that RecA is involved in the control of expression of the pWW0-encoded Pol V.In natural environments, bacteria are faced with many different types of stresses. Among them, nutritional stress is the most common for bacteria occupying various water and soil habitats (71). Additionally, environmental bacteria are frequently exposed to cycles of drying and rehydration. Microorganisms living in geographic areas where the temperature sometimes drops below zero are faced with series of freezing and melting. Many bacteria, especially those living in a phyllosphere, are exposed to UV irradiation. The UV wavelengths that reach the earth's surface can cause direct DNA damage by inducing the formation of DNA photoproducts whose accumulation can be lethal to cells through the blockage of DNA replication and RNA transcription (45). Some data published already more than 20 years ago indicate that freeze-thaw stress and drying cycles can also cause DNA damage which is mutagenic to a bacterium (3,10,65,73). It has also been shown that oxidative DNA damage generated from endogenous metabolism in growth-arrested cells accumulates during stasis (7,8).In Escherichia coli, DNA polymerases Pol II, Pol IV, and Pol V are induced as part of the SOS regulon in response to DNA damage (23). The LexA repressor binds to a 20-bp consensus sequence in the operator region of the SOS regulon genes, suppressing their expression. RecA/single-stranded DNA nucleoprotein filament functions as a coprotease that stimulates LexA autoproteolysis (37). The timing, duration, and level of expression can vary for each LexA-regulated gene, depending on the location and binding affinity of the SOS boxes relative to the strength of the promoter. Therefore, some genes may be part...

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Section: Resultsmentioning

confidence: 75%

“…Many plasmids possess the ability to increase the survival and mutation rates of their UV-irradiated bacterial host (22,25,32,33,35,38,50,53,(58)(59)(60)79). These phenotypes are connected with the presence of genes exhibiting homology to E. coli umuDC genes.…”

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confidence: 99%

A DNA Polymerase V Homologue Encoded by TOL Plasmid pWW0 Confers Evolutionary Fitness on Pseudomonas putida under Conditions of Environmental Stress

et al. 2005

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“…Indeed, the abundance of chromogenic species common to the phyllosphere (e.g., Erwinia herbicola [renamed Pantoea agglomerans; however, we will refer to the bacterium by the more familiar name E. herbicola], xanthomonads, fluorescent pseudomonads, and pink-pigmented facultative methylotrophs) has led to the yet unresolved speculation that pigment production may confer a selective advantage to bacteria that colonize a habitat which is exposed to solar radiation daily (58,182,251,272). At present there is some effort under way to determine if UV radiation affects the survival or fitness of bacteria in the phyllosphere (273). Once the importance of solar radiation to survival of bacteria adapted to the phyllosphere is better understood, the importance of pigmentation in this process may become better resolved.…”

Section: The Playersmentioning

confidence: 99%

Bacteria in the Leaf Ecosystem with Emphasis onPseudomonas syringae—a Pathogen, Ice Nucleus, and Epiphyte

Hirano

Upper

2000

Microbiol Mol Biol Rev

822

610

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SUMMARY The extremely large number of leaves produced by terrestrial and aquatic plants provide habitats for colonization by a diversity of microorganisms. This review focuses on the bacterial component of leaf microbial communities, with emphasis on Pseudomonas syringae—a species that participates in leaf ecosystems as a pathogen, ice nucleus, and epiphyte. Among the diversity of bacteria that colonize leaves, none has received wider attention than P. syringae, as it gained notoriety for being the first recombinant organism (Ice− P. syringae) to be deliberately introduced into the environment. We focus on P. syringae to illustrate the attractiveness and somewhat unique opportunities provided by leaf ecosystems for addressing fundamental questions of microbial population dynamics and mechanisms of plant-bacterium interactions. Leaf ecosystems are dynamic and ephemeral. The physical environment surrounding phyllosphere microbes changes continuously with daily cycles in temperature, radiation, relative humidity, wind velocity, and leaf wetness. Slightly longer-term changes occur as weather systems pass. Seasonal climatic changes impose still a longer cycle. The physical and physiological characteristics of leaves change as they expand, mature, and senesce and as host phenology changes. Many of these factors influence the development of populations of P. syringae upon populations of leaves. P. syringae was first studied for its ability to cause disease on plants. However, disease causation is but one aspect of its life strategy. The bacterium can be found in association with healthy leaves, growing and surviving for many generations on the surfaces of leaves as an epiphyte. A number of genes and traits have been identified that contribute to the fitness of P. syringae in the phyllosphere. While still in their infancy, such research efforts demonstrate that the P. syringae-leaf ecosystem is a particularly attractive system with which to bridge the gap between what is known about the molecular biology of genes linked to pathogenicity and the ecology and epidemiology of associated diseases as they occur in natural settings, the field.

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“…Interestingly, the insertion loci of mutants 613 and 618 showed sequence homologies, respectively, to the UV resistance locus rulAB of P. syringae (Sundin et al, 1996) and to the uvrA region of Micrococcus luteus (Shiota & Nakayama, 1989), which both may represent stressinducible genetic loci. To test this, both mutants were screened for impaired resistance to UV irradiation (Fig.…”

Section: Transposon Mutants With Increased Reporter Gene Expression Amentioning

confidence: 99%

Temperature-responsive genetic loci in the plant pathogen Pseudomonas syringae pv. glycinea The GenBank accession numbers for the nucleotide sequences of mutants 560, 561, 562, 563, 564, 568, 570, 574, 590, 591, 593, 596, 599, 601, 605, 608, 613, 617, 618, 626 and 632 determined in this work are AF274322–AF274342, respectively.

et al. 2000

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Plant-pathogenic bacteria may sense variations in environmental factors, such as temperature, to adapt to plant-associated habitats during pathogenesis or epiphytic growth. The bacterial blight pathogen of soybean, Pseudomonas syringae pv. glycinea PG4180, preferentially produces the phytotoxin coronatine at 18 SC and infects the host plant under conditions of low temperature and high humidity. A miniTn5-based promoterless glucuronidase (uidA) reporter gene was used to identify genetic loci of PG4180 preferentially expressed at 18 or 28 SC. Out of 7500 transposon mutants, 61 showed thermoregulated uidA expression as determined by a three-step screening procedure. Two-thirds of these mutants showed an increased reporter gene expression at 18 SC whilst the remainder exhibited higher uidA expression at 28 SC. MiniTn5-uidA insertion loci from these mutants were subcloned and their nucleotide sequences were determined. Several of the mutants induced at 18 SC contained the miniTn5-uidA insertion within the 328 kb coronatine biosynthetic gene cluster. Among the other mutants with increased uidA expression at 18 SC, insertions were found in genes encoding formaldehyde dehydrogenase, short-chain dehydrogenase and mannuronan C-5-epimerase, in a plasmid-borne replication protein, and in the hrpT locus, involved in pathogenicity of P. syringae. Among the mutants induced at 28 SC, insertions disrupted loci with similarities to a repressor of conjugal plasmid transfer, UV resistance determinants, an isoflavanoid-degrading enzyme, a HU-like DNAbinding protein, two additional regulatory proteins, a homologue of bacterial adhesins, transport proteins, LPS synthesis enzymes and two proteases. Genetic loci from 13 mutants did not show significant similarities to any database entries. Results of plant inoculations showed that three of the mutants tested were inhibited in symptom development and in planta multiplication rates. Temperature-shift experiments suggested that all of the identified loci showed a rather slow induction of expression upon change of temperature.

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Resistance to ultraviolet light in Pseudomonas syringae: sequence and functional analysis of the plasmid-encoded rulAB genes

Cited by 60 publications

References 16 publications

A DNA Polymerase V Homologue Encoded by TOL Plasmid pWW0 Confers Evolutionary Fitness on Pseudomonas putida under Conditions of Environmental Stress

A DNA Polymerase V Homologue Encoded by TOL Plasmid pWW0 Confers Evolutionary Fitness on Pseudomonas putida under Conditions of Environmental Stress

Bacteria in the Leaf Ecosystem with Emphasis onPseudomonas syringae—a Pathogen, Ice Nucleus, and Epiphyte

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