Plant microbiomes / Phyllosphere microbiology
The phyllosphere, which is dominated by leaves, represents one of the largest terrestrial habitats for microorganisms, which influence their hosts with respect to growth and resistance to abiotic and biotic stresses. In addition, the microbiota that resides on the roughly one billion square kilometers of global leaf surfaces is sufficiently abundant to impact the global carbon and nitrogen cycles. Apart from its ecological and economic importance, the phyllosphere is also an excellent model habitat to study microbial physiology and adaptation. A long-term perspective of our laboratory is a systems-level understanding of the phyllosphere, with the aims of identifying organizing principles and ultimately developing predictive capabilities at the levels of the system and individual community members.
In our earlier work, we established cultivation-independent metaproteogenomic approaches to study natural phyllosphere (meta-) communities of microorganisms present on different plant host species. This strategy provided us with insights into the overall bacterial community composition and allowed us to identify abundant proteins as a proxy for characteristic proteins and functions of individual community members in the habitat. Our studies revealed a high consistency in bacterial communities at higher taxonomic ranks, and this consistency was also reflected in the metaproteomes of the microbiota on different plant species. Complementary analyses revealed that microbial communities of individual plant hosts are similar within a given environment.
We pioneered the use of synthetic microbial communities and gnotobiotic plant systems to study factors involved in microbe-microbe-plant interactions in the phyllosphere. We established a representative strain collection of leaf isolates from healthy Arabidopsis plants that can be used to establish causal relationships in reductionist approaches. We use isolates and synthetic communities to test for their ability to protect against the foliar plant pathogen Pseudomonas syringae pv. tomato DC3000 on Arabidopsis thaliana. Moreover, we analyze the colonization patterns of bacterial populations in the phyllosphere, with the ultimate goal of establishing assembly rules of bacterial communities in situ. Another current project concerns the identification of host factors that shape the composition of the bacterial community.
Selected Publications
Vogel CM, Potthoff DB, Schäfer M, Barandun N, Vorholt JA (2021) Protective role of the Arabidopsis leaf microbiota against a bacterial pathogen. Nat Microbiol 6, 1537–1548. https://doi.org/10.1038/s41564-021-00997-7 [external pageAbstract]
Massoni J, Bortfeld-Miller M, Widmer A, Vorholt JA (2021) Capacity of soil bacteria to reach the phyllosphere and convergence of floral communities despite soil microbiota variation. Proc Natl Acad Sci USA;118(41):e2100150118. doi: 10.1073/pnas.2100150118. [external pageAbstract]
Pfeilmeier JS, Petti GC, Bortfeld-Miller M, Daniel B, Field CM, Sunagawa S, Vorholt JA (2021) The plant NADPH oxidase RBOHD is required for microbiota homeostasis in leaves. Nat Microbiol. (2021) Jul;6(7):852-864. [external pageAbstract]
Maier BA, Kiefer P, Field CM, Hemmerle L, Bortfeld-Miller M, Emmenegger B, Schäfer M, Pfeilmeier S, Sunagawa S, Vogel CM, Vorholt JA (2021) A general non-self-response as part of plant immunity. Nat Plants. 7:696-705. [external pageAbstract]
Hemmerle L, Ochsner AM, Vonderach T, Hattendorf B, Vorholt JA (2021) Mass spectrometry-based approaches to study lanthanides and lanthanide-dependent proteins in the phyllosphere. Methods Enzymol. 650:215-236. [external pageAbstract]
Massoni J, Bortfeld-Miller M, Jardillier L, Salazar G, Sunagawa S, Vorholt JA (2020) Consistent host and organ occupancy of phyllosphere bacteria in a community of wild herbaceous plant species. ISME J. 1:245-258 [external pageAbstract]
Carlström CI, Field CM, Bortfeld-Miller M, Müller B, Sunagawa S, Vorholt JA (2019) Synthetic microbiota reveal priority effects and keystone strains in the Arabidopsis phyllosphere. Nat Ecol Evol. 10:1445-1454. [external pageAbstract]
Helfrich EJN, Vogel CM, Ueoka R, Schäfer M, Ryffel F, Müller DB, Probst S, Kreuzer M, Piel J, Vorholt JA (2018) Bipartite interactions, antibiotic production and biosynthetic potential of the Arabidopsis leaf microbiome. Nature Microbiology 3: 909–919 [external pageAbstract]
Gottschlich L, Bortfeld-Miller M, Gäbelein C, Dintner S, Vorholt JA (2018) Phosphorelay through the bifunctional phosphotransferase PhyT controls the general stress response in an alphaproteobacterium. PLoS Genet 14(4): e1007294. [external pageAbstract]
Vorholt JA, Vogel C, Carlström CI, Müller DB (2017) Establishing causality: Opportunities of synthetic communities for plant microbiome research. Cell Host Microb. 22:142-155 [external pageAbstract]
Müller DB, Schubert OT, Röst O, Aebersold R, Vorholt JA (2016) Systems-level proteomics of two ubiquitous leaf commensals reveals complementary adaptive traits for phyllosphere colonization. Mol Cell Proteomics. 15.10:3256-3269 [external pageAbstract]
Vogel C, Bodenhausen N, Gruissem W, Vorholt JA (2016) The Arabidopsis leaf transcriptome reveals distinct but also overlapping responses to colonization by phyllosphere commensals and pathogen infection with impact on plant protection. New Phytologist 212:192-207. [external pageAbstract]
Bai Y, Müller DB, Srinivas G, Garrido-Oter R, Potthoff E, Rott M, Dombrowski N, Münch PC, Spaepen S, Remus-Emsermann M, Hüttel B, McHardy AC, Vorholt JA, Schulze-Lefert P (2015) Functional overlap of the Arabidopsis leaf and root microbiota. Nature 528:364-9. [external pageAbstract]
Ryffel F, Helfrich EJN, Kiefer P, Peyriga L, Portais J-C, Piel J, Vorholt JA (2016) Metabolic footprint of epiphytic bacteria on Arabidopsis thaliana leaves. ISME J. 10:632-43 [external pageAbstract]
Bodenhausen N, Bortfeld-Miller M, Ackermann M, Vorholt JA (2014) A synthetic community approach reveals plant genotypes affecting the phyllosphere microbiota. PLoS Genetics 10:e1004283 external page[Abstract]
Remus-Emsermann M, Lücker S, Müller DB, Potthoff E, Daims H, Vorholt JA (2014) Spatial distribution analyses of natural phyllosphere-colonizing bacteria on Arabidopsis thaliana revealed by fluorescence in situ hybridization. Environ. Microbiol. 16:2329-40 external page[Abstract]
Stiefel P, Zambelli T, Vorholt JA (2013) Isolation of optically targeted single bacteria by application of fluidic force microscopy to aerobic anoxygenic phototrophs from the phyllosphere. Appl Environ Microbiol. 79:4895-4905 external page[Abstract]
Vorholt JA (2012) Microbial life in the phyllosphere. Nature Rev Microbiol. 10:828-840 external page[Abstract]
Vogel C, Innerebner G, Zingg J, Guder J, Vorholt JA (2012) A forward genetic in planta screen for the identification of plant-protective traits of Sphingomonas sp. Fr1 against Pseudomonas syringae DC3000. Appl. Environ. Microbiol. 78:5529-5535 external page[Abstract]
Knief C, Delmotte N, Chaffron S, Stark M, Innerebener G, Wassmann R, von Mering C, Vorholt JA (2012) Metaproteogenomic analysis of microbial communities in the phyllosphere and rhizosphere of rice. ISME J. 6:1378-1390 external page[Abstract]
Innerebner G, Knief C, Vorholt JA (2011) Protection of Arabidopsis thaliana against leaf-pathogenic Pseudomonas syringae by Sphingomonas strains in a controlled model system. Appl. Environ. Microbiol. 77:3202-3210 external page[Abstract]
Knief C, Ramette A, Frances L, Blanco CA, Vorholt JA (2010) Site and plant species are important determinants of the Methylobacterium community composition in the plant phyllosphere. ISME J. 4:719-728 [external pageAbstract]
Knief C, Frances L, Vorholt JA (2010) Competitiveness of diverse Methylobacterium strains in the phyllosphere of Arabidopsis thaliana and identification of representative models, including M. extorquens PA1. Microb. Ecol. 60:440-452 external page[Abstract]
Delmotte N, Knief C, Chaffron S, Innerebner G, Roschitzki B, Schlapbach R, von Mering C, Vorholt JA (2009) Community proteogenomics reveals insights into the physiology of phyllosphere bacteria. Proc. Natl. Acad. Sci USA 106:16428-16433 external page[Abstract]