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Bonkowski, M.

Publications and source records attributed to Bonkowski, M..

At least 19 recordsLinked to original sources

Dryland soil rewetting induces strong VOC emissions with potential to form ozone and aerosols

Biogenic volatile organic compounds (VOCs) significantly influence atmospheric chemistry, yet the importance of microbial VOC emissions remains understudied. We investigate petrichor VOC emissions, the characteristic scent following rainfall after prolonged drought, in an aridity gradient across Israel, by simulating soil rewetting events. Rewetting triggered strong VOC fluxes (1-3.5 nmol m-2 s-1 ground area) dominated by sesquiterpenes and benzenoids, with emission patterns linked to climatic regions, soil aridity, and microbial community composition. Petrichor consisted of a complex bouquet of 58 VOCs, and the initial VOC burst resembled the CO2 pulse of the Birch effect. Petrichor emissions showed ozone and secondary organic aerosol formation potentials comparable in magnitude to those estimated for anthropogenic VOC sources in Israel. Despite compositional differences, emissions were of similar magnitudes across the aridity gradient. Given that drylands cover nearly half of Earths terrestrial surface and are expanding, these episodic microbial VOC emissions may represent a significant, previously overlooked source of reactive carbon with potential implications for regional and global atmospheric chemistry.

microbiology↗

Earthworm invasion reduces above-belowground biodiversity and ecosystem multifunctionality

Global change alters abiotic and biotic conditions across the globe with unprecedented consequences for the functional integrity of affected ecosystems. However, most studies addressing global-change impacts focus on a very limited number of environmental variables, taxa, and ecosystem functions. Evidence is mounting that many belowground ecosystems are subject to an underappreciated aspect of global change: the invasion of earthworms. While we know that earthworm invasion can impact the physical, chemical, and biological properties of invaded ecosystems, it remains poorly understood how these changes are interconnected and how they concurrently affect the overall functioning of an ecosystem. To fill this gap, we collected data on six environmental variables, ten functional groups of microbes, plants, and animals, and 16 ecosystem functions from four forests in the USA and Canada, well-known hotspots of earthworm invasion. We used a multi-step Structural-Equation Modeling approach to disentangle the direct and indirect effects of earthworm invasion on environmental conditions and the ecosystem multidiversity and multifunctionality of invaded forests at different levels of resolution. Our analysis revealed that earthworm invasion reduced total multidiversity (combined microbial, plant, and animal multidiversity). Ecosystem multifunctionality was reduced via a combination of direct and indirect effects, with the latter involving both effects mediated by altered environmental conditions and by total multidiversity. In contrast, when resolving total multidiversity into taxon-specific multidiversity indices for microbes, plants, and animals, the above-mentioned effects of earthworm invasion on multifunctionality via multidiversity disappeared. Invasion effects on single ecosystem functions differed in their mediators but were net negative across the board. Given these differences across the differently-resolved analyses, the results suggest that a whole- ecosystem perspective is paramount to comprehensively understanding the impacts of biological invasions. Combining a multi-step analytical design with multiple biodiversity indices and multiple ecosystem functions assessed at the same time and place, our study represents the most complete assessment of the mechanisms and ecosystem-level consequences of earthworm invasion to date.

ecology↗

Physiological diversity and adaptation of Rhizaria revealed by phylogenomics and comparative transcriptomics

Protists are vastly diverse, forming over 20 supergroups of the eukaryotic diversity and fulfilling plentiful functions. Rhizaria is a widespread and highly abundant supergroup comprising important parasites and a huge diversity of free-living heterotrophic predators. Despite the diversity and biogeochemical importance of Rhizaria, our understanding of their physiology and metabolic capabilities remains limited, mainly due to a general lack of data and bioinformatic tools for cross-species comparisons of physiological traits. In this study, we assembled a total of 15 transcriptomes of the parasite-related bacterivorous Rhogostoma and their eukaryvorous relatives. By phylogenomic analyses and whole transcriptome comparison, we established an evolutionary framework to which we relate physiological traits. The morphologically highly similar Rhogostoma strains branch in two distinct clusters differing in orthogroups and gene expression patterns related to cell adhesion and biofilm formation. Furthermore, we reveal considerable intra-genus variation in amino acid and lipid metabolism, which might be explained by an ancient streamlining through gradual specialization to parasitism, bearing the potential for subsequent metabolic radiation. We conclude that even closely related and morphologically similar species in Rhizaria may differ distinctly in their functional repertoire. With the here established and showcased analyses, we create a basis for future characterization of the physiological traits of microeukaryotes.

microbiology↗

Differential contributions of an antimicrobial effector from Verticillium dahliae to virulence and tomato microbiota assembly across natural soils

Throughout their life cycle plants associate with diverse and complex microbial communities, known as their microbiota. These microbiota contribute to plant performance and health, in part by providing a microbial barrier against invading plant pathogens. To colonize plant hosts, pathogens not only have to overcome host immune responses, but also breach the microbial barrier, for which they secrete so-called effector proteins. Accordingly, the soil-borne fungal plant pathogen Verticillium dahliae secretes the antimicrobial effector Ave1 to suppress antagonistic microbes and facilitate host colonization. Notably, many pathogens, including V. dahliae, have life stages outside their host plants, for instance in soil, where they encounter diverse microbial communities. Yet, how antimicrobial effectors support establishment across these environments remains poorly understood. To address this, we established a collection of natural soil samples with diverse physicochemical properties and microbiota compositions. Using this collection, we show for three plant species, barley, tomato and cotton, that root-associated bacterial and fungal communities are primarily shaped by the type of soil, whereas the phyllosphere microbiota is mainly determined by plant species. On tomato, we furthermore show that Ave1 differentially contributes to virulence on diverse soils, as Ave1 altered the tomato microbiota on all soils tested, but the taxa affected by these shifts varied depending on the specific soils. Our findings suggest that while Ave1-mediated microbiota manipulation occurs across soils, its impact on fungal virulence is influenced by the specific composition of the soil-derived microbiota assembled by the host.

plant biology↗

Plant diversity shapes plant volatile emission differently at the species and community level

Studies have investigated the interactions between plants through competition and resource sharing to understand the mechanisms behind the positive effects of plant diversity on productivity. Volatile organic compounds (VOCs) are important info-chemicals in plant-plant interactions, but they have so far rarely been considered in this context. Here, we measured VOC emissions at both community and species levels (Plantago lanceolata) in experimental plant communities of varying diversity (The Jena Experiment) to understand the role of VOCs in driving biodiversity-ecosystem functioning relationships. We show that plant diversity determines the release of plant VOCs at both levels. At the community level, plant species richness directly enhanced VOC emission and increased VOC richness both directly and indirectly by altering herbivore damage and LAI. At the species level, plant diversity did not directly affect the VOC emissions of P. lanceolata but indirectly affected it by influencing the VOC emissions from the surrounding community. Plantago lanceolata individuals in communities with high concentrations of green leaf volatiles decreased their VOC emission, while those in communities with high concentrations of terpenoids increased their VOC diversity. Our results provide first evidence that plant diversity shapes community-level plant VOC emission and thus influences focal plant VOC emission inside the community.

ecology↗

A novel protistan trait database reveals functional redundancy and complementarity in terrestrial protists (Amoebozoa & Rhizaria)

The inclusion of functional traits of protists in environmental sequencing surveys, in addition to the traditional taxonomic framework, is essential for a better understanding of their roles and impacts on ecosystem processes. We provide a database of functional traits for a widespread and important clade of protists, the Amoebozoa, based on extensive literature research in eight trait categories: Habitat, locomotion, nutrition, morphology, morphotype, size, spore formation, and disease-relatedness. The comparison of community traits of the Amoebozoa with sympatric but highly divergent Cercozoa (Rhizaria) revealed both convergent evolution of morphology or locomotion and distinct differences in habitat preference and feeding selectively. Amoebozoa seem to be rather unselective in their prey choice compared to Cercozoa. Indeed, the feeding preferences of Amoebozoa appeared to be related to cell size, whereas Cercozoa selectively feed on prey. Applications to metatranscriptomic data from soil, litter, and bark surfaces revealed differences in the average community trait compositions and ecosystem functioning, such as an increased proportion of disease-related Amoebozoa in soil or different proportions of nutrition types of Amoebozoa and Cercozoa on bark. This database will facilitate ecological analyses of sequencing data and improve our understanding of the diversity of adaptations of Amoebozoa to the environment and their functional roles in ecosystems.

ecology↗

Microbial utilisation of maize rhizodeposits applied to an agricultural soil at a range of concentrations

Rhizodeposition fuels carbon (C) and nutrient cycling in soil. However, the dynamics of microbial growth on rhizodeposits in relation to the distance from the root have not been well studied. This study investigates microbial growth on individual organic components of rhizodeposits and on maize root-derived exudates and mucilage from an agricultural soil. By creating a gradient of substrate concentrations, we simulated reduced microbial access to rhizosphere C with increasing distance to the root surface. We identified distinct C-thresholds for the activation of microbial growth, and these were significantly higher for rhizodeposits compared to singular, simple sugars. In addition, testing for stoichiometric constraints of microbial growth by supplementing N and P showed accelerated and increased microbial growth by activating a larger proportion of the microbial biomass. Early and late season exudates triggered significantly different microbial growth responses. The mineralisation of early season exudates was induced at a high C-threshold, whereas the mineralisation of late season exudates showed sugar-like properties, with a low C-threshold, high substrate affinity, and a reduced maximum respiration rate. Mucilage exhibited the highest C-threshold for the activation of microbial growth, although with a short lag-period and with an efficient mucilage degradation comparable to that of sugars. By determining kinetic parameters and turnover times for different root-derived substrates, our data enable the upscaling of micro-scale processes to the whole root system, allowing more precise predictions of how rhizodeposits drive microbial C and nutrient dynamics in soil. HighlightsO_LIGrowth thresholds for rhizodeposits were significantly higher than for singular, simple sugars. C_LIO_LINo distinct microbial growth on root exudates was observed even at high concentrations. C_LIO_LIMucilage has a short lag-phase and efficient decomposition like sugars but only above a high threshold. C_LIO_LIN and P limited microbial growth in the agricultural soil. C_LI

ecology↗

Fungivorous protists in the rhizosphere of Arabidopsis thaliana - Diversity, functions, and publicly available cultures for experimental exploration

In the context of the soil food web, the transfer of plant-fixed energy and carbon to higher trophic levels has traditionally been attributed to two main energy channels: the fungal energy channel and the bacterial energy channel. Historically, protists were overlooked in the fungal energy channel, which was believed to be controlled by fungivorous microarthropods and nematodes. In this study, we investigated fungivorous protists in the rhizosphere of Arabidopsis thaliana. Our findings revealed a notable abundance and diversity of protists that have developed specialized strategies to overcome the protective cell wall of fungi. Among the identified species were two Vampyrellida (Rhizaria) species, namely Theratromyxa weberi and Platyreta germanica, as well as one Arcellinida (Amoebozoa) species, called Cryptodifflugia oviformis. While T. weberi typically consumed entire fungal cells, the other two species perforated fungal cell walls and extracted the cellular contents. We elucidate the feeding strategies and dietary ranges of the amoebae, highlighting the non-uniform nature of fungivory in protists, as different taxa have evolved distinct approaches to access fungi as a food source. Moreover, we provide publicly available cultures of these protists to facilitate further experimental investigations within the research community.

ecology↗

A fast-slow trait continuum at the level of entire communities

Across the tree of life, organismal functional strategies form a continuum from slow-to fast-growing organisms, in response to common drivers such as resource availability and disturbance. However, the synchronization of these strategies at the entire community level is untested. We combine trait data for >2800 above-and belowground taxa from 14 trophic guilds spanning a disturbance and resource availability gradient in German grasslands. Most guilds consistently respond to these drivers through both direct and trophically-mediated effects, resulting in a slow-fast axis at the level of the entire community. Fast trait communities were also associated with faster rates of whole ecosystem functioning. These findings demonstrate that slow and fast strategies can be manifested at the level of whole ecosystems, opening new avenues of ecosystem-level functional classification.

ecology↗

Biotic interactions explain seasonal dynamics of the alpine soil microbiome

BackgroundThe soil alpine microbiome is dependent on season and elevation, yet there is limited understanding of how complex communities are differentially shaped by abiotic and biotic factors. Here we investigated the spring-to-summer dynamics of soil microbiomes in alpine grasslands, focussing on soil food web interactions. To this end, we conducted a survey along altitudinal transects in three mountains in the Alps, in spring at snowmelt and in the following summer, recorded vegetation and topographic, climatic and edaphic parameters for 158 soil samples. By using metatranscriptomics, we simultaneously assessed prokaryotic and eukaryotic communities, further classified by nutrition guilds. ResultsOur results show: (i) that biotic interactions could explain more variation of the microbial communities than topographic and edaphic variables, more for consumers than for preys, and this effect was stronger in summer than in spring; (ii) a seasonal dynamic in biotic interactions: the consumers pressure on preys increases from spring to summer, resulting in a higher diversity and evenness of preys. ConclusionIn alpine grasslands, consumers effectively contribute to maintain the diverse soil bacterial and fungal community essential for ecosystem functioning.

ecology↗

Linking rhizosphere processes across scales: Opinion

PurposeSimultaneously interacting small-scale rhizosphere processes determine emergent plant-scale behaviour, including growth, transpiration, nutrient uptake, soil carbon storage and transformation by microorganisms. Current advances in modelling and experimental methods open the path to unravel and link those processes. MethodsWe present a series of examples of state-of-the art simulations addressing this multi-scale, multi-process problem from a modelling point of view, as well as from the point of view of integrating newly available rhizosphere data and images. ResultsEach example includes a model that links scales and experimental data to set-up simulations that explain and predict spatial and temporal distribution of rhizodeposition as driven by root architecture development, soil structure, presence of root hairs, soil water content and distribution of soil water. Furthermore, two models explicitly simulate the impact of the rhizodeposits on plant nutrient uptake and soil microbial activity, respectively. This exemplifies the currently available state of the art modelling tools in this field: image-based modelling, pore-scale modelling, continuum scale modelling and functional-structural plant modelling. We further show how to link the pore scale to the continuum scale by homogenisation or by deriving effective physical parameters like viscosity from nano-scale chemical properties. ConclusionModelling allows to integrate and make use of new experimental data across different rhizosphere processes (and thus across different disciplines) and scales. Described models are tools to test hypotheses and consequently improve our mechanistic understanding of how rhizosphere processes impact plant-scale behaviour. Linking multiple scales and processes is the logical next step for future research.

bioengineering↗

A parasite's paradise: Biotrophic species prevail oomycete community composition in tree canopies

Oomycetes (Stramenopiles, Protista) are among the most severe plant pathogens, comprising species with a high economic and ecologic impact on forest ecosystems. Their diversity and community structures are well studied in terrestrial habitats, but tree canopies as huge and diverse habitats have been widely neglected. A recent study highlighted distinct oomycete communities in the canopy region compared to forest soils when taking oomycete abundances into account, in contrast to the homogeneity at the incidence level. It remains however unknown if this homogeneity also leads to a functional homogenisation among microhabitats. In this study, we supplemented functional traits to oomycete canopy and ground communities, which were determined over a time period of two years with a metabarcoding approach. Our results showed that even though most oomycetes occurred in all habitats, a strong discrepancy between the strata and correspondingly the distribution of oomycete lifestyles could be observed, which was constant over time. Obligate biotrophic species, exclusively feeding on living host tissue, dominated the canopy region, implying tree canopies to be a hitherto neglected reservoir for parasitic protists. Parasites highly specialised on hosts that were not sampled could be determined in high abundances in the canopy and the surrounding air, challenging the strict host dependencies ruled for some oomycetes. Our findings further contribute to the understanding of oomycete ecosystem functioning in forest ecosystems.

microbiology↗

On the phenology of protists: Recurrent patterns reveal seasonal variation of protistan (Rhizaria: Cercozoa, Endomyxa) communities in tree canopies

Tree canopies are colonized by billions of highly specialized microorganisms that are well adapted to the extreme microclimatic conditions, caused by diurnal fluctuations and seasonal changes. In this study we investigated seasonality patterns of protists in tree canopies of a temperate floodplain forest via high-throughput sequencing with group-specific primers for the phyla Cercozoa and Endomyxa. We observed consistent seasonality and identified divergent spring and autumn taxa. Tree crowns were characterized by a dominance of bacterivores and omnivores, while eukaryvores gained a distinctly larger share in litter and soil communities on the ground. Seasonality was largest among communities detected on the foliar surface. Higher variance within alpha diversity of foliar communities in spring indicated greater heterogeneity during community assembly. However, communities underwent distinct changes during the aging of leaves in autumn, reflecting recurring phenological changes during microbial colonization of leaves. Surprisingly, endomyxan root pathogens appeared to be exceptionally abundant across tree canopies during autumn season, demonstrating a potential role of the canopy surface as an important reservoir for wind-dispersed propagules. Overall, about 80% of detected OTUs could not be assigned to known species - representing only a fraction of dozens of microeukaryotic taxa whose canopy inhabitants are waiting to be discovered.

ecology↗

To the canopy and beyond: Air samples reveal wind dispersal as a driver of ubiquitous protistan pathogen assembly in tree canopies

We analyzed air dispersal of the protistan phyla Cercozoa and Oomycota with an air sampler near the ground (~2 m) and in tree crowns (~25 m) of three tree species (oak, linden and ash) in a temperate floodplain forest in March (before leafing) and May (after leaf unfolding) with a cultivation-independent high throughput metabarcoding approach. Both, Cercozoa and Oomycota, contain important pathogens of forest trees and other vegetation. We found a high diversity of Cercozoa and Oomycota in air samples with 122 and 81 OTUs, respectively. Especially oomycetes showed a high temporal variation in beta diversity between both sampling dates. Differences in community composition between air samples in tree canopies and close to the ground were however negligible, and also tree species identity did not affect communities in air samples, indicating that the distribution of protistan propagules through the air was not spatially restricted in the forest ecosystem. OTUs of plant pathogens, whose host species that did not occur in the forest, demonstrate wind dispersal of propagules from outside the forest biome. Overall, our results lead to a better understanding of the stochastic processes of wind dispersal of protists and protistan pathogens, a prerequisite to understand the mechanisms of their community assembly in forest ecosystems. ImportanceWind dispersal has been shown to play a crucial role in protistan community assembly. The protistan taxa Cercozoa and Oomycota contain important plant parasites with a major ecologic and economic impact. However, comprehensive assessments of cercozoan and oomycete diversity in forest air samples were lacking. Using a cultivation-independent high throughput metabarcoding approach, we analyzed cercozoan and oomycete air dispersal in forest floors and the canopy region - a potential filter for microbial propagules. Our study provides insights into the diversity and community assembly of protists within the air, contributing to a better understanding which factors drive the distribution of plant pathogens within forest ecosystems.

ecology↗

Distinct responses of oomycete plant parasites according to their lifestyle in a landscape-scale metabarcoding survey

Oomycetes are an ubiquitous protistan lineage including devastating crop parasites. Although their ecology in agrosystems has been widely studied, little is known of their distribution in natural and semi-natural ecosystems. We provide here a baseline of the diversity and distribution of soil oomycetes, classified by lifestyles (biotrophy, hemibiotrophy and saprotrophy), at the landscape scale in temperate grassland and forest. From 600 soil samples, we obtained 1,148 Operational Taxonomy Units representing [~]20 million Illumina reads (region V4, 18S rRNA gene). We found a majority of hemibiotrophic plant pathogens, which are parasites spending part of their life cycle as saprotrophs after the death of the host. Overall both grassland and forest constitute an important reservoir of plant pathogens. In forests, relative abundances of obligate biotrophs and hemibiotrophs differed between regions and showed opposite responses to edaphic conditions and human-induced management intensification, suggesting different ecological requirements for these two functional guilds.

ecology↗

Contrasting responses of protistan plant parasites and phagotrophs to ecosystems, land management and soil properties

Functional traits are increasingly used in ecology to link the structure of microbial communities to ecosystem processes. We investigated two important protistan lineages, Cercozoa and Endomyxa (Rhizaria) in soil using Illumina sequencing and analysed their diversity and functional traits along with their responses to environmental factors in grassland and forest across Germany. From 600 soil samples, we obtained 2,101 Operational Taxonomy Units representing ~18 million Illumina reads (region V4, 18S rRNA gene). All major taxonomic and functional groups were present, dominated by small bacterivorous flagellates (Glissomonadida). Endomyxan plant parasites were absent from forest. In grassland, they were promoted by more intensive land use management. Grassland and forest strikingly differed in community composition. Relative abundances of bacterivores and eukaryvores were contrastingly influenced by environmental factors, indicating bottom-up regulation by food resources. These patterns provide new insights into the functional organization of soil biota and indications for a more sustainable land-use management. HighlightsO_LIProtistan plant parasites of worldwide importance (Phytomyxea) are absent from forest C_LIO_LIProtistan plant parasites are enhanced by land use intensification in grassland C_LIO_LIOpposite responses of protistan trophic guilds to environmental conditions in forest C_LIO_LIDrastic differences in protistan community composition between grassland and forest C_LI

ecology↗

What drives the assembly of plant-associated protist microbiomes?

In a field experiment we investigated the influence of the environmental filters soil type and plant species identity on rhizosphere community assembly of Cercozoa, a dominant group of (mostly bacterivorous) soil protists. The experiment was set up with two plant species, lettuce and potato, grown in an experimental plot system with three contrasting soils. Plant species (14%) and rhizosphere origin (vs. bulk soil) with 13%, together explained four times more variation in cercozoan beta diversity than the three soil types (7% explained variation in beta diversity). Our results clearly confirm the existence of plant species-specific protist communities. Network analyses of bacteria-Cercozoa rhizosphere communities identified scale-free small world topologies, indicating mechanisms of self-organization. While the assembly of rhizosphere bacterial communities is bottom-up controlled through the resource supply from root (secondary) metabolites, our results support the hypothesis that the net effect may depend on the strength of top-down control by protist grazers. Since grazing of protists has a strong impact on the composition and functioning of bacteria communities, protists expand the repertoire of plant genes by functional traits, and should be considered as protist microbiomes in analogy to bacterial microbiomes. HighlightMicrobiomes of rhizosphere protists are plant species-specific and tightly co-evolving with their bacterial prey, thereby extending and modifying the functional repertoire of the bacterial-plant symbiosis.

plant biology↗

Environmental selection and spatiotemporal structure of a major group of soil protists (Rhizaria: Cercozoa) in a temperate grassland

Soil protists are increasingly appreciated as essential components of soil foodwebs; however, there is a dearth of information on the factors structuring their communities. Here we investigate the importance of different biotic and abiotic factors as key drivers of spatial and seasonal distribution of protistan communities. We conducted an intensive survey of a 10m2 grassland plot in Germany, focusing on a major group of protists, the Cercozoa. From 177 soil samples, collected from April to November, we obtained 694 Operational Taxonomy Units representing >6 million Illumina reads. All major cercozoan groups were present, dominated by the small flagellates of the Glissomonadida. We found evidence of environmental filtering structuring the cercozoan communities both spatially and seasonally. Spatial analyses indicated that communities were correlated within a range of four meters. Seasonal variations of bactevirores and bacteria, and that of omnivores after a time-lapse, suggested a dynamic prey-predator succession. The most influential edaphic properties were moisture and clay content, which differentially affected each functional group. Our study is based on an intense sampling of protists at a small scale, thus providing a detailed description of the niches occupied by different taxa/functional groups and the ecological processes involved.

ecology↗