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Wippel, K.

Publications and source records attributed to Wippel, K..

9 recordsLinked to original sources

Experimental evolution of root-associated microbial communities

Microbial communities associated with plants are dynamic ecosystems whose structure and functions influence host health and fitness. While the ecological roles and beneficial function of plant microbiomes are increasingly well understood, the evolutionary dynamics that shape them over time remain unclear. Experimental evolution constitutes a powerful tool to study microbial adaptation, but so far, its application has been largely focused on free-living or single-species populations. Here, we use experimental evolution to test whether taxonomically complex synthetic bacterial communities can adapt to novel plant hosts. We show that replicate microbial communities undergo rapid and parallel genomic evolution, with measurable gains in colonization fitness. Adaptive changes involved mutations in regulatory processes, motility, and core metabolism, leading to significant fitness gains across diverse taxa. Our findings demonstrate that the plant host can drive microbiome evolution without disrupting the stability of the root microbiota.

microbiology↗

Bacteria rewire fungal antimicrobial gene expression in microbial arms races

Microbial communities are shaped by antagonistic interactions, yet how competitors evade antimicrobial strategies in a community context remains unclear. Fungi deploy antimicrobial proteins (AMPs) to suppress bacterial niche competitors, but how bacteria counteract these defences is unknown. Here we show that soil microbiota suppress fungal AMP expression, revealing a previously unrecognized mode of intermicrobial interference. In the soil-borne pathogen Verticillium dahliae, AMP genes are highly conserved yet broadly repressed in the presence of natural microbial communities. This repression extends across diverse fungi, suggesting a widespread phenomenon. Correlation analyses of AMP expression and community compositions linked the bacterial genera Leptothrix and Devosia to repression of the V. dahliae AMPs VdL1 and VdD1, respectively. Both AMPs antagonize these bacterial taxa, and microbiota-mediated repression of VdL1 reduces its contribution to fungal soil colonization. Together, our findings reveal that bacteria can evade fungal antagonism by suppressing AMP deployment, highlighting community-level control of microbial competition.

microbiology↗

A gnotobiotic system reveals multifunctional effector roles in plant-fungal pathogen dynamics

Plants host diverse microbiota that influence physiological processes and can enhance resilience against invading pathogens that, in turn, evolved effector proteins to manipulate host microbiota in their favor. However, the complexity of microbial communities and their interactions complicates mechanistic research on processes governing microbiota assembly and function. Gnotobiotic systems are valuable tools to study plant microbiota by reducing complexity and enabling controlled microbiota reconstitution experiments. Despite their utility, no gnotobiotic systems have been established to investigate the role of antimicrobial effector proteins in the interactions between plants, their microbiota, and fungal pathogens. Here, we present a refined gnotobiotic system designed to study these interactions, establishing protocols for infections with the fungal pathogen Verticillium dahliae across multiple host plants under sterile conditions. We demonstrate that a synthetic microbial community (SynCom) derived from a culture collection generated for this study can be applied in this system where it interferes with fungal infections. Additionally, using our gnotobiotic system we reveal that specific antimicrobial effectors of V. dahliae, like Ave1L2, contribute to fungal virulence in a microbiota-dependent manner, whereas other antimicrobial effectors, such as Ave1, seem to possess functions beyond microbiota manipulation.

plant biology↗

Pseudomonas intra-genus competition determines protective function of SynComs in Arabidopsis thaliana

The plant root microbiota is crucial for nutrient acquisition, development, and disease suppression. Although commensal bacteria display host preference, their beneficial impact on their cognate host and mechanisms of species selection by the plant are still unclear. We use bacterial culture collections derived from the two model species Arabidopsis thaliana (At) and Lotus japonicus (Lj) to design synthetic communities (SynComs) and test their protective function upon exposure of At Col-0 to the detrimental root-colonizing Pseudomonas isolate R401. Lj-derived SynComs were fully protective, whereas At-derived SynComs displayed full protective activity only towards a R401 mutant impaired in the production of inhibitory exometabolites. The protective phenotypes were associated with a reduced titer of the R401 opportunistic pathogen. In vitro antagonist assays, in planta and in vitro bacterial community profiling, as well as strain-swapping and strain-dropout experiments revealed that competition among commensal Pseudomonas strains and R401 determines the success of the opportunist, independent of the original host or the phylogeny of the commensals. Furthermore, we determine the carbon utilization potential of these isolates, which may explain the competition with the detrimental strain and the role of host-secreted compounds. Our results provide evidence that intra-genus interactions within SynComs modulate plant health and disease, and that an individual beneficial strain can be sufficient to outcompete an opportunistic relative. This has implications for the successful development of beneficial microbial consortia for agriculture.

plant biology↗

Multi-laboratory Study Establishes Reproducible Methods for Plant-Microbiome Research in Fabricated Ecosystems

Inter-laboratory replicability is crucial yet challenging in microbiome research. Leveraging microbiomes to promote soil health and plant growth requires understanding underlying molecular mechanisms using reproducible experimental systems. In a global collaborative effort involving five laboratories, we aimed to help advance reproducibility in microbiome studies by testing our ability to replicate synthetic community assembly experiments. Our study compared fabricated ecosystems constructed using two different synthetic bacterial communities, the model grass Brachypodium distachyon, and sterile EcoFAB 2.0 devices. All participating laboratories observed consistent inoculum-dependent changes in plant phenotype, root exudate composition, and final bacterial community structure where Paraburkholderia sp. OAS925 could dramatically shift microbiome composition. Comparative genomics and exudate utilization linked the pH-dependent colonization ability of Paraburkholderia, which was further confirmed with motility assays. The study provides detailed protocols, benchmarking datasets, and best practices to help advance replicable science and inform future multi-laboratory reproducibility studies.

microbiology↗

Timing of root barriers controls soil-to-shoot integration of rhizosphere status

In roots, formation of the Casparian strip in the endodermal cell walls provides a mechanism for selective uptake of nutrients and water. Establishment of this filter is under spatial surveillance by a receptor-ligand mechanism termed the Schengen pathway. This system provides a mechanism to initiate downstream signaling responses in case of dysfunctional barrier establishment. Due to this interconnected nature, the endogenous physiological role of this survaillance mechanism remain difficult to untangle from the direct barrier function. This is in particularly evident in complex growth setups where multiple inputs are integrated into general whole-plant responses. In this work, we address this by rewiring the genetic network that underlies root barrier formation. We create plants with enhanced, Schengen-independent Casparian strip formation that are not only suitable to probe the role of stronger barrier establishment, but also to evaluate the associated signaling output independently. With focus on the latter, we subjected the rewired plants, as well as a number of established barrier mutants, to multifaceted growth conditions including nitrogen fertilized agricultural soil conditions. By profiling their above- and belowground (a)biotic responses our work reveals that, while increased Casparian strip formation mainly provides the plant with an improved stress resistance, the Schengen pathway is necessary for establishment of a growth-promoting root microbiome and serves to convey information of soil nitrogen status to the shoot. This identifies the Schengen pathway as an essential receptor-based signaling hub for adaptive integration of barrier status, nutritional responses and (a)biotic signaling between above- and belowground tissues.

plant biology↗

Modulation of Arabidopsis growth by volatile organic compounds from a root-derived bacterial community

Plant roots are surrounded by fluctuating biotic and abiotic factors. The living component - the microbiota - is actively shaped by the plant and plays an important role in overall plant health. While it has been shown that specialized metabolites exuded from the plant are involved in shaping host interactions with the microbiota, it is unclear how underground volatile organic compounds (VOCs) influence this communication. This is especially true for root-associated bacteria which are known to release VOCs that can influence plant growth. Using a simplified synthetic bacterial community (SynCom) representing the phylogenetic diversity of bacteria in the root microbiome, we set out to characterize plant growth and defense metabolites when subjected to bacterial VOCs (bVOCs). Moreover, by profiling the SynCom community composition after co-cultivation with the plant, we explored how members of the community influenced each other in our growth setup. Our findings reveal that plant growth promotion can occur via VOCs from a bacterial SynCom, but that the plant response differs for individual community members. In addition, we find that bVOCs are able to repress chemical defense responses in the plant, possibly to facilitate colonization. By removing key species from the SynCom, we find that complex bacteria-bacteria interactions are likely to underlie this phenomenon, and that bVOC-induced modulation of plant responses in the rhizosphere may be an emergent property of bacterial communities rather than depending on individual species.

plant biology↗

Characterization of the Chlamydomonas reinhardtii phycosphere reveals conserved features of the plant microbiota

Microscopic algae release organic compounds to the region immediately surrounding their cells, known as the phycosphere, constituting a niche for colonization by heterotrophic bacteria. These bacteria take up algal photoassimilates and provide beneficial functions to their host, in a process that resembles the establishment of microbial communities associated with the roots and rhizospheres of land plants. Here, we characterize the microbiota of the model alga Chlamydomonas reinhardtii and reveal extensive taxonomic and functional overlap with the root microbiota of land plants. Reconstitution experiments using synthetic communities derived from C. reinhardtii and Arabidopsis thaliana show that phycosphere and root bacteria assemble into taxonomically equivalent communities on either host. We show that provision of diffusible metabolites is not sufficient for phycosphere community establishment, which additionally requires physical proximity to the host. Our data suggests that the microbiota of photosynthetic organisms, including green algae and flowering plants, assembles according to core ecological principles.

microbiology↗

Host preference and invasiveness of commensals in the Lotus and Arabidopsis root microbiota

Healthy plants are colonized by microorganisms from the surrounding environment, which form stable communities and provide beneficial services to the host. Culture-independent profiling of the bacterial root microbiota shows that different plant species are colonized by distinct bacterial communities, even if they share the same habitat. It is, however, not known to what extent the host actively selects these communities and whether commensal bacteria are adapted to a specific plant species. Here, we report a sequence-indexed culture collection from roots and nodules of the model legume Lotus japonicus that contains representatives from the majority of species found in culture-independent profiles. Using taxonomically paired synthetic communities from L. japonicus and the crucifer Arabidopsis thaliana in a multi-species gnotobiotic system, we detect clear signatures of host preference among commensal bacteria in a community context, but not in mono-associations. Sequential inoculation of either host reveals strong priority effects during the assembly of the root microbiota, where established communities are resilient to invasion by late-comers. However, we found that host preference by commensal bacteria confers a competitive advantage in their native host. We reveal that host preference is prevalent in commensal bacteria from diverse taxonomic groups and that this trait is directly linked to their invasiveness into standing root-associated communities.

plant biology↗