Dataset Information

Correlated production and consumption of chloromethane in the Arabidopsis thaliana phyllosphere.

ABSTRACT: Chloromethane (CH3Cl) is a toxic gas mainly produced naturally, in particular by plants, and its emissions contribute to ozone destruction in the stratosphere. Conversely, CH3Cl can be degraded and used as the sole carbon and energy source by specialised methylotrophic bacteria, isolated from a variety of environments including the phyllosphere, i.e. the aerial parts of vegetation. The potential role of phyllospheric CH3Cl-degrading bacteria as a filter for plant emissions of CH3Cl was investigated using variants of Arabidopsis thaliana with low, wild-type and high expression of HOL1 methyltransferase previously shown to be responsible for most of CH3Cl emissions by A. thaliana. Presence and expression of the bacterial chloromethane dehalogenase cmuA gene in the A. thaliana phyllosphere correlated with HOL1 genotype, as shown by qPCR and RT-qPCR. Production of CH3Cl by A. thaliana paralleled HOL1 expression, as assessed by a fluorescence-based bioreporter. The relation between plant production of CH3Cl and relative abundance of CH3Cl-degrading bacteria in the phyllosphere suggests that CH3Cl-degrading bacteria co-determine the extent of plant emissions of CH3Cl to the atmosphere.

SUBMITTER: Farhan Ul Haque M

PROVIDER: S-EPMC5730606 | biostudies-literature | 2017 Dec

REPOSITORIES: biostudies-literature

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Correlated production and consumption of chloromethane in the Arabidopsis thaliana phyllosphere.

Farhan Ul Haque Muhammad M Besaury Ludovic L Nadalig Thierry T Bringel Françoise F Mutterer Jérôme J Schaller Hubert H Vuilleumier Stéphane S

Scientific reports 20171214 1

Chloromethane (CH3Cl) is a toxic gas mainly produced naturally, in particular by plants, and its emissions contribute to ozone destruction in the stratosphere. Conversely, CH3Cl can be degraded and used as the sole carbon and energy source by specialised methylotrophic bacteria, isolated from a variety of environments including the phyllosphere, i.e. the aerial parts of vegetation. The potential role of phyllospheric CH3Cl-degrading bacteria as a filter for plant ...[more]

PMID: 29242530

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Project description:UnlabelledBacteria living on the aerial parts of plants (the phyllosphere) are globally abundant and ecologically significant communities and can have significant effects on their plant hosts. Despite their importance, little is known about the ecological processes that drive phyllosphere dynamics. Here, we describe the development of phyllosphere bacterial communities over time on the model plant Arabidopsis thaliana in a controlled greenhouse environment. We used a large number of replicate plants to identify repeatable dynamics in phyllosphere community assembly and reconstructed assembly history by measuring the composition of the airborne community immigrating to plant leaves. We used more than 260,000 sequences from the v5v6 hypervariable region of the 16S rRNA gene to characterize bacterial community structure on 32 plant and 21 air samples over 73 days. We observed strong, reproducible successional dynamics: phyllosphere communities initially mirrored airborne communities and subsequently converged to a distinct community composition. While the presence or absence of particular taxa in the phyllosphere was conserved across replicates, suggesting strong selection for community composition, the relative abundance of these taxa was highly variable and related to the spatial association of individual plants. Our results suggest that stochastic events in early colonization, coupled with dispersal limitation, generated alternate trajectories of bacterial community assembly within the context of deterministic selection for community membership.ImportanceCommensal bacteria associated with plants help protect their hosts against infection and promote growth. Bacteria associated with plant leaves (the "phyllosphere") are highly abundant and diverse communities, but we have very limited information about their ecology. Here, we describe the formation of phyllosphere communities on the plant model organism Arabidopsis thaliana. We grew a large number of plants in a greenhouse and measured bacterial diversity in the phyllosphere throughout the Arabidopsis life cycle. We also measured the diversity of airborne microbes landing on leaves. Our findings show that plants develop distinctive phyllosphere bacterial communities drawn from low-abundance air populations, suggesting the plant environment is favorable for particular organisms and not others. However, we also found that the relative abundances of bacteria in the phyllosphere are determined primarily by the physical proximity of individual plants. This suggests that a mixture of selective and random forces shapes phyllosphere communities.

Project description:Biosurfactant production is a common trait in leaf surface-colonizing bacteria that has been associated with increased survival and movement on leaves. At the same time, the ability to degrade aliphatics is common in biosurfactant-producing leaf colonizers. Pseudomonads are common leaf colonizers and have been recognized for their ability to produce biosurfactants and degrade aliphatic compounds. In this study, we investigated the role of biosurfactants in four non-plant-pathogenic Pseudomonas strains by performing a series of experiments to characterize their surfactant properties and their role during leaf colonization and diesel degradation. The biosurfactants produced were identified using mass spectrometry. Two strains produced viscosin-like biosurfactants, and the other two produced massetolide A-like biosurfactants, which aligned with the phylogenetic relatedness between the strains. To further investigate the role of surfactant production, random Tn5 transposon mutagenesis was performed to generate knockout mutants. The knockout mutants were compared to their respective wild types with regard to their ability to colonize gnotobiotic Arabidopsis thaliana and to degrade diesel or dodecane. It was not possible to detect negative effects during plant colonization in direct competition or individual colonization experiments. When grown on diesel, knockout mutants grew significantly slower than their respective wild types. When grown on dodecane, knockout mutants were less impacted than during growth on diesel. By adding isolated wild-type biosurfactants, it was possible to complement the growth of the knockout mutants.IMPORTANCE Many leaf-colonizing bacteria produce surfactants and are able to degrade aliphatic compounds; however, whether surfactant production provides a competitive advantage during leaf colonization is unclear. Furthermore, it is unclear if leaf colonizers take advantage of the aliphatic compounds that constitute the leaf cuticle and cuticular waxes. Here, we tested the effect of surfactant production on leaf colonization, and we demonstrate that the lack of surfactant production decreases the ability to degrade aliphatic compounds. This indicates that leaf surface-dwelling, surfactant-producing bacteria contribute to degradation of environmental hydrocarbons and may be able to utilize leaf surface waxes. This has implications for plant-microbe interactions and future studies.

Dataset Information

Correlated production and consumption of chloromethane in the Arabidopsis thaliana phyllosphere.

Publications

Correlated production and consumption of chloromethane in the Arabidopsis thaliana phyllosphere.

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