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Pseudomonas syringae Increases Water Availability in Leaf Microenvironments via Production of Hygroscopic Syringafactin.

ABSTRACT: The epiphytic bacterium Pseudomonas syringae strain B728a produces the biosurfactant syringafactin, which is hygroscopic. The water-absorbing potential of syringafactin is high. Syringafactin attracts 250% of its weight in water at high relative humidities but is less hygroscopic at lower relative humidities. This finding suggests that the benefit of syringafactin to the producing cells is strongly context dependent. The contribution of syringafactin to the water availability around cells on different matrices was assessed by examining the water stress exhibited by biosensor strains expressing gfp via the water-stress-activated proU promoter. Wild-type cells exhibited significantly less green fluorescent protein (GFP) fluorescence than a syringafactin-deficient strain on dry filters in atmospheres of high water saturation, as well as on leaf surfaces, indicating greater water availability. When infiltrated into the leaf apoplast, wild-type cells also subsequently exhibited less GFP fluorescence than the syringafactin-deficient strain. These results suggest that the apoplast is a dry but humid environment and that, just as on dry but humid leaf surfaces, syringafactin increases liquid water availability and reduces the water stress experienced by P. syringae IMPORTANCE Many microorganisms, including the plant pathogen Pseudomonas syringae, produce amphiphilic compounds known as biosurfactants. While biosurfactants are known to disperse hydrophobic compounds and to reduce water tension, they have other properties that can benefit the cells that produce them. Leaf-colonizing bacteria experience frequent water stress, since liquid water is present only transiently on or in leaf sites that they colonize. The demonstration that syringafactin, a biosurfactant produced by P. syringae, is sufficiently hygroscopic to increase water availability to cells, thus relieving water stress, reveals that P. syringae can modify its local habitat both on leaf surfaces and in the leaf apoplast. Such habitat modification may be a common role for biosurfactants produced by other bacterial species that colonize habitats (such as soil) that are not always water saturated.

SUBMITTER: Hernandez MN

PROVIDER: S-EPMC6715840 | biostudies-literature | 2019 Sep

REPOSITORIES: biostudies-literature

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Pseudomonas syringae Increases Water Availability in Leaf Microenvironments via Production of Hygroscopic Syringafactin.

Hernandez Monica N MN Lindow Steven E SE

Applied and environmental microbiology 20190829 18

The epiphytic bacterium <i>Pseudomonas syringae</i> strain B728a produces the biosurfactant syringafactin, which is hygroscopic. The water-absorbing potential of syringafactin is high. Syringafactin attracts 250% of its weight in water at high relative humidities but is less hygroscopic at lower relative humidities. This finding suggests that the benefit of syringafactin to the producing cells is strongly context dependent. The contribution of syringafactin to the water availability around cells ...[more]

PMID: 31285194

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Project description:UNLABELLED:The plant pathogen Pseudomonas syringae pv. syringae B728a grows and survives on leaf surfaces and in the leaf apoplast of its host, bean (Phaseolus vulgaris). To understand the contribution of distinct regulators to B728a fitness and pathogenicity, we performed a transcriptome analysis of strain B728a and nine regulatory mutants recovered from the surfaces and interior of leaves and exposed to environmental stresses in culture. The quorum-sensing regulators AhlR and AefR influenced few genes in planta or in vitro. In contrast, GacS and a downstream regulator, SalA, formed a large regulatory network that included a branch that regulated diverse traits and was independent of plant-specific environmental signals and a plant signal-dependent branch that positively regulated secondary metabolite genes and negatively regulated the type III secretion system. SalA functioned as a central regulator of iron status based on its reciprocal regulation of pyoverdine and achromobactin genes and also sulfur uptake, suggesting a role in the iron-sulfur balance. RetS functioned almost exclusively to repress secondary metabolite genes when the cells were not on leaves. Among the sigma factors examined, AlgU influenced many more genes than RpoS, and most AlgU-regulated genes depended on RpoN. RpoN differentially impacted many AlgU- and GacS-activated genes in cells recovered from apoplastic versus epiphytic sites, suggesting differences in environmental signals or bacterial stress status in these two habitats. Collectively, our findings illustrate a central role for GacS, SalA, RpoN, and AlgU in global regulation in B728a in planta and a high level of plasticity in these regulators' responses to distinct environmental signals. IMPORTANCE:Leaves harbor abundant microorganisms, all of which must withstand challenges such as active plant defenses and a highly dynamic environment. Some of these microbes can influence plant health. Despite knowledge of individual regulators that affect the fitness or pathogenicity of foliar pathogens, our understanding of the relative importance of various global regulators to leaf colonization is limited. Pseudomonas syringae strain B728a is a plant pathogen and a good colonist of both the surfaces and interior of leaves. This study used global transcript profiles of strain B728a to investigate the complex regulatory network of putative quorum-sensing regulators, two-component regulators, and sigma factors in cells colonizing the leaf surface and leaf interior under stressful in vitro conditions. The results highlighted the value of evaluating these networks in planta due to the impact of leaf-specific environmental signals and suggested signal differences that may enable cells to differentiate surface versus interior leaf habitats.

Dataset Information

Pseudomonas syringae Increases Water Availability in Leaf Microenvironments via Production of Hygroscopic Syringafactin.

Publications

Pseudomonas syringae Increases Water Availability in Leaf Microenvironments via Production of Hygroscopic Syringafactin.

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