Abstract:
Plants form complex and dynamic interactions with diverse microbial communities of beneficial, neutral, and pathogenic microorganisms spanning multiple phylogenetic kingdoms. The structures of plant-associated microbial communities vary due to a broad range of factors such as plant host, environment, and other assembly processes occurring at multiple tempo-spatial scales. In natural environments plant microbial communities are constantly exposed to such abiotic and biotic perturbations and ecological processes. Thus, to attain a systemic understanding of the ecology of plant microbiomes, it is essential to study microbial communities associated with plants in natural environments and understand the assembly processes that influence patterns of microbial community structures. In this study we examined the ecology of microbiomes in natural populations of Lotus corniculatus. Specifically, we investigated the effect of plant organs, plant age and genotype, as well as environmental factors on the diversity and composition of the natural plant microbiome. We collected soil and plant samples for four consecutive years across seven wild populations in Southern Germany and analyzed the bacterial, fungal, and eukaryotic communities associated with soil and L. corniculatus roots, shoots, flowers, and seeds.
In this study we established the organ-specificity of plant endophytic communities. Therefore, we used the framework of metacommunity theory of ecology to understand assembly processes that shape community structures by defining microbial communities associated with the roots, shoots, flowers, and seeds as distinct communities linked by dispersal. The plant microbiomes are shaped by selective filtering of the plant organs as demonstrated by the differential abundance and persistence of microbes in roots, shoots, flowers, and seeds. The plant organs can be distinguished with separator microbes that we identified using multi-class support vector machine models. The community structure of the plant microbiomes is further influenced by microbial interactions, as well as by local abiotic and biotic factors. These distinct yet overlapping organ microbial communities are linked and shaped by transmission of microorganisms among the plant compartments and the local environment.
In this study we also observed spatial and temporal variation in L. corniculatus microbiomes at multiple scales, therefore we examined how abiotic and biotic factors in the local environment influence the structure of natural microbiomes. We show that plant microbiomes are shaped by a set of environmental factors that are distinct to each plant compartment. Moreover, we found that soil temperature seasonality, soil microbiome composition, air temperature seasonality, plant community richness, and grazing influence the structure and microbial interactions in the plant organs. These environmental factors are different in their association with each compartment’s microbiomes, possibly influencing dispersal decisions of microorganisms and consequently contribute in shaping distinct yet overlapping microbiomes across plant organs. We also detected organ-dependent environmental perception in generalist plant microbes as well as in organ biomarker microbes.
Finally, in this study we observed that the natural L. corniculatus populations exhibit variations in age and genotype, therefore we investigated the effect of these plant host- related factors on the associated microbial communities. We show that plant age and genotype significantly influence the structure of associated microbiomes. While a large number of taxa are shared among plant genotype and age groups, we identified biomarker microbes that distinguish between host genotypes or age groups through differential abundance analysis. Based on these findings, we isolated Fusarium from wild L. corniculatus plants and showed that this plant pathogen, which is significantly more abundant in one genotype, elicited stronger response in the offspring of plants of this genotype compared with the offspring of plants of another genotype.
Understanding the ecological processes that shape microbial assembly and community dynamics in natural environments is crucial in leveraging the benefits of plant microbiomes on plant productivity, resilience, and pathogen defense. Knowledge about the organ-specific responses of plant microbiomes to abiotic and biotic perturbations will provide an important framework for targeted control of plant microbiomes in the context of global climate change. Observed patterns on dispersal decisions or habitat choice of microorganisms based on organ-dependent environmental cues and microbial interactions also advance our insight on how beneficial microbes or pathogens survive and persist on specific plant microhabitats or environmental conditions. Finally, knowledge on how plant age and genotype impact associated microbial communities, as well as detection of microbial biomarkers at specific plant age or genotype, provide clues as to how the spread of pathogen can be mitigated in the future or how infection-resistant plants can be developed.
plant microbiomes