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This article is a Commentary on Mark et al. (2020), 227: 1362–1375.

The importance of microbial root inhabitants for plant growth and health was recognized as early as 100 years ago. Recent insights reveal a close symbiotic relationship between plants and their associated microorganisms, and high structural and functional diversity within plant microbiomes. Plants provide microbial communities with specific habitats, which can be broadly categorized as the rhizosphere, phyllosphere, and endosphere. Plant-associated microbes interact with their host in essential functional contexts. They can stimulate germination and growth, help plants fend off disease, promote stress resistance, and influence plant fitness. Therefore, plants have to be considered as metaorganisms within which the associated microbes usually outnumber the cells belonging to the plant host. The structure of the plant microbiome is determined by biotic and abiotic factors but follows ecological rules. Metaorganisms are co-evolved species assemblages. The metabolism and morphology of plants and their microbiota are intensively connected with each other, and the interplay of both maintains the functioning and fitness of the holobiont. Our study of the current literature shows that analysis of plant microbiome data has brought about a paradigm shift in our understanding of the diverse structure and functioning of the plant microbiome with respect to the following: (i) the high interplay of bacteria, archaea, fungi, and protists; (ii) the high specificity even at cultivar level; (iii) the vertical transmission of core microbiomes; (iv) the extraordinary function of endophytes; and (v) several unexpected functions and metabolic interactions. The plant microbiome should be recognized as an additional factor in experimental botany and breeding strategies.

Lichen symbioses develop long-living thallus structures even in the harshest environments on Earth. These structures are also habitats for many other microscopic organisms, including other fungi, which vary in their specificity and interaction with the whole symbiotic system. This contribution reviews the recent progress regarding the understanding of the lichen-inhabiting fungi that are achieved by multiphasic approaches (culturing, microscopy, and sequencing). The lichen mycobiome comprises a more or less specific pool of species that can develop symptoms on their hosts, a generalist environmental pool, and a pool of transient species. Typically, the fungal classes Dothideomycetes, Eurotiomycetes, Leotiomycetes, Sordariomycetes, and Tremellomycetes predominate the associated fungal communities. While symptomatic lichenicolous fungi belong to lichen-forming lineages, many of the other fungi that are found have close relatives that are known from different ecological niches, including both plant and animal pathogens, and rock colonizers. A significant fraction of yet unnamed melanized (‘black’) fungi belong to the classes Chaethothyriomycetes and Dothideomycetes. These lineages tolerate the stressful conditions and harsh environments that affect their hosts, and therefore are interpreted as extremotolerant fungi. Some of these taxa can also form lichen-like associations with the algae of the lichen system when they are enforced to symbiosis by co-culturing assays.

Microscopic and molecular studies suggest that lichen symbioses contain a plethora of associated fungi. These are potential producers of novel bioactive compounds, but strains isolated on standard media usually represent only a minor subset of these fungi. By using various in vitro growth conditions we are able to modulate and extend the fraction of culturable lichen-associated fungi. We observed that the presence of iron, glucose, magnesium and potassium in growth media is essential for the successful isolation of members from different taxonomic groups. According to sequence data, most isolates besides the lichen mycobionts belong to the classes Dothideomycetes and Eurotiomycetes. With our approach we can further explore the hidden fungal diversity in lichens to assist in the search of novel compounds.

Background Arugula is a traditional medicinal plant and popular leafy green today. It is mainly consumed raw in the Western cuisine and known to contain various bioactive secondary metabolites. However, arugula has been also associated with high-profile outbreaks causing severe food-borne human diseases. A multiphasic approach integrating data from metagenomics, amplicon sequencing, and arugula-derived bacterial cultures was employed to understand the specificity of the indigenous microbiome and resistome of the edible plant parts. Results Our results indicate that arugula is colonized by a diverse, plant habitat-specific microbiota. The indigenous phyllosphere bacterial community was shown to be dominated by Enterobacteriaceae, which are well-equipped with various antibiotic resistances. Unexpectedly, the prevalence of specific resistance mechanisms targeting therapeutic antibiotics (fluoroquinolone, chloramphenicol, phenicol, macrolide, aminocoumarin) was only surpassed by efflux pump assignments. Conclusions Enterobacteria, being core microbiome members of arugula, have a substantial implication in the overall resistome. Detailed insights into the natural occurrence of antibiotic resistances in arugula-associated microorganisms showed that the plant is a hotspot for distinctive defense mechanisms. The specific functioning of microorganisms in this unusual ecosystem provides a unique model to study antibiotic resistances in an ecological context.

This study introduces a novel methodology to explore the network dynamics of Physarum polycephalum , an organism celebrated for its remarkable adaptive capabilities. We used two innovative techniques to analyse its growth behaviour and network modifications under stress conditions, including starvation and differential epinephrine exposures. The first method provided a quantitative assessment of growth and exploration over time. The second method provided a detailed examination of vein diameter and contraction patterns, illuminating the physiological adjustments P. polycephalum undergoes in response to environmental challenges. By integrating these approaches, we were able to estimate the total network volume of the organism, with a focus on the normalized estimated volume, unveiling insightful aspects of its structural adaptations. While starvation reduced the volume, indicating a significant structural compromise, low and high epinephrine concentrations maintained a volume-to-area ratio comparable with the control. Determining the fractal dimension of the networks over time revealed a fine-tuning of the network complexity in response to environmental conditions, with significant reductions under stress indicating a constrained network adaptation strategy. These methods, novel in their application to P. polycephalum , provide a framework for future studies and a basis for exploring complex network behaviours with potential applications in bioengineering and adaptive network design.

Salt is essential for life, though excessive intake disrupts the balance of body fluids in multicellular organisms like humans. We wondered what happens when body fluids circulate in a single cell. To address this question, we studied the effects of excessive salt on the network-forming giant cell of the slime mold Physarum polycephalum . We analyse the phenotypic and transcriptomic responses during exposure of plasmodia to various concentrations of sodium chloride. Morphological observations revealed alterations in the tubular network architecture, including reduced network vein diameter and changes in typical peristaltic contraction frequency. Transcriptomic analysis identified more than 2000 differentially expressed genes, with a significant upregulation of ion transporters, membrane proteins and stress-related pathways, alongside with a downregulation of genes involved in metabolic degradation. These findings suggest that P. polycephalum mitigates salt stress by regulating ion homeostasis, adjusting cytoskeletal dynamics and modulating gene expression related to cellular defence mechanisms. Possible alterations of the secreted slime coat and corresponding mechanical feedback mechanisms are discussed. The insights into the salt stress responses of P. polycephalum help to understand the salt response of a protist that is evolutionary basal to animals and fungi.

Symbioses represent a frequent and successful lifestyle on earth and lichens are one of their classic examples. Recently, bacterial communities were identified as stable, specific and structurally integrated partners of the lichen symbiosis, but their role has remained largely elusive in comparison to the well-known functions of the fungal and algal partners. We have explored the metabolic potentials of the microbiome using the lung lichen Lobaria pulmonaria as the model. Metagenomic and proteomic data were comparatively assessed and visualized by Voronoi treemaps. The study was complemented with molecular, microscopic and physiological assays. We have found that more than 800 bacterial species have the ability to contribute multiple aspects to the symbiotic system, including essential functions such as (i) nutrient supply, especially nitrogen, phosphorous and sulfur, (ii) resistance against biotic stress factors (that is, pathogen defense), (iii) resistance against abiotic factors, (iv) support of photosynthesis by provision of vitamin B 12 , (v) fungal and algal growth support by provision of hormones, (vi) detoxification of metabolites, and (vii) degradation of older parts of the lichen thallus. Our findings showed the potential of lichen-associated bacteria to interact with the fungal as well as algal partner to support health, growth and fitness of their hosts. We developed a model of the symbiosis depicting the functional multi-player network of the participants, and argue that the strategy of functional diversification in lichens supports the longevity and persistence of lichens under extreme and changing ecological conditions.

Background and AimsThe integrity and evolution of lichen symbioses depend on a fine-tuned combination of algal and fungal genotypes. Geographically widespread species complexes of lichenized fungi can occur in habitats with slightly varying ecological conditions, and it remains unclear how this variation correlates with symbiont selectivity patterns in lichens. In an attempt to address this question, >300 samples were taken of the globally distributed and ecologically variable lichen-forming species complex Tephromela atra, together with closely allied species, in order to study genetic diversity and the selectivity patterns of their photobionts.MethodsLichen thalli of T. atra and of closely related species T. grumosa, T. nashii and T. atrocaesia were collected from six continents, across 24 countries and 62 localities representing a wide range of habitats. Analyses of genetic diversity and phylogenetic relationships were carried out both for photobionts amplified directly from the lichen thalli and from those isolated in axenic cultures. Morphological and anatomical traits were studied with light and transmission electron microscopy in the isolated algal strains.Key ResultsTephromela fungal species were found to associate with 12 lineages of Trebouxia. Five new clades demonstrate the still-unrecognized genetic diversity of lichen algae. Culturable, undescribed lineages were also characterized by phenotypic traits. Strong selectivity of the mycobionts for the photobionts was observed in six monophyletic Tephromela clades. Seven Trebouxia lineages were detected in the poorly resolved lineage T. atra sensu lato, where co-occurrence of multiple photobiont lineages in single thalli was repeatedly observed.ConclusionsLow selectivity apparently allows widespread lichen-forming fungi to establish successful symbioses with locally adapted photobionts in a broader range of habitats. This flexibility might correlate with both lower phylogenetic resolution and evolutionary divergence in species complexes of crustose lichen-forming fungi.

Lettuce cultivars are not only amongst the most popular vegetables eaten raw, they are also involved in severe pathogen outbreaks world-wide. While outbreaks caused by Enterobacteriaceae species are well-studied, less is known about their occurrence in natural environments as well as the impact of biotic stress. Here, we studied the ecology of the human health-relevant bacterial family Enterobacteriaceae and assessed the impact of biotic disturbances by a soil-borne phytopathogenic fungus and Gastropoda on their structure and abundance in mesocosm and pot experiments. Using a polyphasic approach including network analyses of 16S rRNA gene amplicon libraries, quantitative PCR and complementary fluorescence in situ hybridization (FISH) microscopy we found substantial yet divergent Enterobacteriaceae communities. A similar spectrum of 14 genera was identified from rhizo- and phyllospheres but the abundance of Enterobacteriaceae was on average 3fold higher in phyllosphere samples. Both stress factors shifted the bacterial community of the leaf habitat, characterized by increases of species abundance and diversity. For the rhizosphere, we observed significant structural shifts of Enterobacteriaceae communities but also a high degree of resilience. These results could be confirmed by FISH microscopy but it was difficult to visualize phyllosphere communities. Additional inoculation experiments with Escherichia coli as model revealed their presence below the wax layer as well as in the endosphere of leaves. The observed presence influenced by stress factors and the endophytic life style of Enterobacteriaceae on lettuce can be an important aspect in relation to human health.