Community proteogenomics reveals insights into the physiology of phyllosphere bacteria

By Nathanaël Delmotte, C. Knief, Samuel Chaffron, G. Innerebner, B. Roschitzki, R. Schlapbach, C. von Mering, Julia A. Vorholt. Proceedings of the National Academy of Sciences of the United States of America, 2009

823 citations recorded by the source corpus.

Aerial plant surfaces represent the largest biological interface on Earth and provide essential services as sites of carbon dioxide fixation, molecular oxygen release, and primary biomass production. Rather than existing as axenic organisms, plants are colonized by microorganisms that affect both their health and growth. To gain insight into the physiology of phyllosphere bacteria under in situ conditions, we performed a culture-independent analysis of the microbiota associated with leaves of soybean, clover, and Arabidopsis thaliana plants using a metaproteogenomic approach. We found a high consistency of the communities on the 3 different plant species, both with respect to the predominant community members (including the alphaproteobacterial genera Sphingomonas and Methylo bacterium) and with respect to their proteomes. Observed known proteins of Methylobacterium were to a large extent related to the ability of these bacteria to use methanol as a source of carbon and energy. A remarkably high expression of various TonB-dependent receptors was observed for Sphingomonas. Because these outer membrane proteins are involved in transport processes of various carbohydrates, a particularly large substrate utilization pattern for Sphingomonads can be assumed to occur in the phyllosphere. These adaptations at the genus level can be expected to contribute to the success and coexistence of these 2 taxa on plant leaves. We anticipate that our results will form the basis for the identification of unique traits of phyllosphere bacteria, and for uncovering previously unrecorded mechanisms of bacteria-plant and bacteria-bacteria relationships.

Subfields: Plant Science

View Paper: https://www.semanticscholar.org/paper/44282f10210d0e05e181e8f970dec116b94f91e6

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Citations in the corpus

• Endophyte research: going beyond isolation and metabolite documentation (2013, background): “Metaproteomics has helped in defining the functional roles of different microbes in complex, multi-microbe communities such as soil (Wang et al., 2011), ground water (Benndorf et al., 2007), leaf surface (Delmotte et al., 2009) and plant litter (Schneider et al., 2012).”
• Bacterial Communities Associated with the Leaves and the Roots of Arabidopsis thaliana (2013, background): “thaliana, all phyla that are typical of the phyllosphere [20,40] and the rhizosphere [21,22,39,41], suggesting substantial overlap in the key commuFigure 3.”
• The ecology of the phyllosphere: geographic and phylogenetic variability in the distribution of bacteria on tree leaves (2010, neutral): “We identified many of the same bacterial taxa found in other culture-independent studies of the phyllosphere, including high relative abundances of lineages within the Bacteroidetes, Actinobacteria and Proteobacteria phyla (Yang et al., 2001; Jackson et al., 2006; Lambais et al., 2006; Delmotte et a”
• Phyllospheric Microbiomes: Diversity, Ecological Significance, and Biotechnological Applications (2020, methodology): “Methylobacterium spp. are involved in the assimilation of methanol at the phyllosphere, a by-product of demethylated pectin during the cell wall metabolism of the plant (Galbally and Kirstine 2002; Delmotte et al. 2009), and it gives epiphytic fitness to the microbes.”
• The plant microbiome (2013, background): “These studies [48,63] also determined that Methylobacterium spp.”
• The Plant Microbiota: Systems-Level Insights and Perspectives. (2016, background): “Besides metabolic capabilities, responses to stress were identified as important functional traits of leaf-colonizing bacteria (29).”
• Simplified and representative bacterial community of maize roots (2017, background): “belonging to Actinobacteria was 1% (67, 68) and increased dramatically to 40% in the synthetic community (26), which led to the finding that the distributions of the Rhodococcus sp.”
• Who is who in litter decomposition? Metaproteomics reveals major microbial players and their biogeochemical functions (2012, background): “, 2007, 2009), and leaf phyllosphere (Delmotte et al., 2009).”
• Managing the ecology of foliar pathogens: ecological tolerance in crops (2010, background): “A greater level of microbial identification can be achieved by coupling high throughput DNA analysis with proteomics analysis (Delmotte et al., 2009).”
• The rhizosphere microbiome: significance of plant beneficial, plant pathogenic, and human pathogenic microorganisms. (2013, background): “A metaproteogenomic approach was first reported for bacterial communities in the phyllosphere of Arabidopsis, soybean, and clover plants (Delmotte et al., 2009).”
• Molecular Techniques to Assess Microbial Community Structure, Function, and Dynamics in the Environment (2011, methodology): “The proteogenomics approach was applied to decipher phyllosphere bacterial communities in a study by Delmotte et al. (2009).”
• Long-term features of cloud microbiology at the puy de Dôme (France) (2012, background): “Microorganisms commonlyaffiliatedwith thephyllosphere includenotably species of Clavibacter, Curtobacterium, Methylobacterium, Pseudomonas, Sphingomonas and Stenotrophomonas in bacteria (Morris et al., 2008; Delmotte et al., 2009) and species of Dioszegia and Cryptococcus in yeasts (Renker et al.”