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Dumack, K.

Publications and source records attributed to Dumack, K..

15 recordsLinked to original sources

A rhizarian genome reveals an osmotrophic route to extracellular digestion in eukaryotes

Rhizaria, one of the most species-rich and ecologically important eukaryotic supergroups, accommodates a newly discovered osmotrophic species, yet high-quality genomic resources remain scarce, limiting our understanding of their metabolic diversity and ecological functions. Here, we present the genome of Saccharomycomorpha psychra, the first rhizarian telomere-anchored assembly, to be explored as a model and reference for rhizarian ecology and evolution. The 62 Mb assembly, of which half comprises 22 telomere-to-telomere scaffolds, shows a BUSCO completeness of 94.2%, encodes 17,680 genes, and provides the genomic foundation for investigating rhizarian ecology and evolution. The genome of osmotrophic Saccharomycomorpha psychra reveals a functionally integrated secretome of 1,015 proteins dominated by carbohydrate-active enzymes (CAZymes), proteases, lipases, and oxidoreductases. Taken together with 303 predicted high-confidence membrane transporters of a total of 680, skewed toward H-coupled secondary carriers, these features constitute the genomic signature of an extracellular digestive strategy convergent with saprotrophic fungi. Phenotypic MicroArrayTM assays confirmed active utilization of 17 carbon sources, including all six C5 pentose sugars tested, consistent with the predicted arabinose and ribokinase pathways among the most highly expressed metabolic genes in the transcriptome. These findings demonstrate that osmotrophic saprotrophy has evolved independently in Rhizaria with enzymatic solutions that closely parallel those of evolutionary distant fungal decomposers, highlighting the power of ecological context over phylogenetic heritage in shaping extracellular metabolic architecture.

genomics↗

Who and how much? Quantifying the role of trophic guilds in soil organic carbon mineralization

Understanding the biotic processes that drive soil organic carbon (SOC) mineralization is essential for predicting the climate warming-carbon cycle feedback. Here, we combined Tree-of-life sequencing (TOLseq; cross-domain profiling using ribosomal RNA) with quantitative conversion factors linking rRNA transcript abundance to biomass, to understand how soil food web changes affect SOC mineralization in an in situ soil warming experiment. Field observations showed that warming reduced SOC stocks, but after decades of warming SOC mineralization had acclimated. An energetic soil food web model revealed both bottom-up and top-down controls in the trophic cascades, shifting C flows from fungal and plant-associated channels towards the bacterial channel. This caused an increase in SOC mineralization rate in warmed soils of 30% per-unit biomass across the year.

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↗

Sea-ice microbial community succession and the potential role of parasitoids in the maintenance of diversity

Sea ice is a crucial, yet declining, habitat in high latitude ecosystems. Here we present a high-temporal resolution amplicon sequence data set collected during the spring ice-algal bloom near Utqia[g]vik, Alaska in 2021 to study sea-ice microbial dynamics. The ice-algal bloom peaked on May 8th, reaching 46.6 mg chlorophyll a m-2, and thereafter became limited by nitrate availability. A massive bloom of the oil-degrading bacterium, Oleispira (>80% relative abundance), coincided with the algal bloom raising questions about hydrocarbon exposure. The sea-ice algal bloom was dominated by diatoms, particularly Nitzschia spp., and transitioned into a flagellate dominated post-bloom community which aligned with melt-associated changes to the physicochemical environment. We explored the relationship between putative parasitoids, Chytridiomycetes, Thecofilosea (Cercozoa), Oomycetes, Syndiniales (Dinoflagellata), and Labyrinthulomycetes (Bigyra), and potential microalgal hosts. Chytrids peaked periodically suggesting synchronized infections and Cryothecomonas (Thecofilosea) was observed parasitizing Nitzschia spp. for the first time in Arctic sea ice. Co-occurrence analysis suggested that diatoms, especially Nitzschia, were the primary hosts of Pacific-Arctic parasitoids, and that top-down parasitoid control may dramatically alter community composition over short timescales, such as days. These results provide important insights into the drivers of spring bloom timing and maintenance of microalgal diversity in sea ice.

microbiology↗

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↗

Lotka-Volterra Dynamics Facilitate Sustainable Biocontrol of Wastewater Sludge Bulking

Biological wastewater treatment is driven by complex interactions between prokaryotes and eukaryotes. Occasionally, filamentous bacteria species, first and foremost Ca. Microthrix parvicella, increase in abundance and lead to detrimental wastewater sludge bulking or floating, causing environmental harm and financial losses. Current mitigation strategies rely heavily on nonspecific chemical interventions, which present environmental risks and lack prolonged effectiveness. Here, we utilise long-term monitoring data from four German wastewater treatment plants (WWTPs) to explore sustainable biocontrol alternatives. Our findings reveal Lotka-Volterra dynamics between Ca. Microthrix parvicella and the protist Arcella spp. Visual and experimental validation demonstrate the suppression of filamentous bacterial growth by predation. We further model these interactions, predicting the biocontrol potential of Arcella spp. for both immediate and sustained efficacy in managing sludge bulking. These results highlight the potential of protists as biological control agents, providing a more sustainable and environmentally friendly alternative to chemical treatment.

ecology↗

Biodiversity in mountain soils above the treeline

Despite the importance of healthy soils for human livelihood, wellbeing, and safety, current gaps in our knowledge and understanding of biodiversity in soil are numerous, undermining conservation efforts. These gaps are particularly wide in mountain regions where healthy soils are especially important for human safety and yet evidence is accumulating of ongoing degradation, posing significant threats to ecosystem functioning and human settlements. To analyse these gaps in detail, we synthesise current research on the global diversity of microorganisms, cryptogams, and invertebrates in mountain soils above the treeline. This synthesis is based on a semi-quantitative survey of the literature and an expert-based analysis. Our work reveals not only deficiencies in geographic cover but also significant gaps in taxonomic coverage, particularly among soil protists and invertebrates, and a lack of (functional and ecological) description of the uncultivated majority of prokaryotes, fungi, and protists. We subsequently build on this overview to highlight opportunities for research on mountain soils as systems of co-occurring species that interact in complex environmental matrices to fulfil critical functions and make essential contributions to life on land. Closing gaps in biodiversity research in mountain soil is crucial to enhance our understanding and to promote laws and guidelines advancing international soil biodiversity conservation targets in mountains. Addressing sparse and biased data, recognizing the impact of environmental changes on mountain ecosystems, and advocating dedicated policies are essential strategies to safeguard mountain soils and their biodiversity. GLOSSARY O_TBL View this table: org.highwire.dtl.DTLVardef@16682fdorg.highwire.dtl.DTLVardef@121b9feorg.highwire.dtl.DTLVardef@139eadeorg.highwire.dtl.DTLVardef@16abd74org.highwire.dtl.DTLVardef@bc3da9_HPS_FORMAT_FIGEXP M_TBL C_TBL

ecology↗

Amoebozoan testate amoebae illuminate the diversity of heterotrophs and the complexity of ecosystems throughout geological time

Heterotrophic protists are vital in Earths ecosystems, influencing carbon and nutrient cycles and occupying key positions in food webs as microbial predators. Fossils and molecular data suggest the emergence of predatory microeukaryotes and the transition to a eukaryote-rich marine environment by 800 million years ago (Ma). Neoproterozoic vase-shaped microfossils (VSMs) linked to Arcellinida testate amoebae represent the oldest evidence of heterotrophic microeukaryotes. This study explores the phylogenetic relationship and divergence times of modern Arcellinida and related taxa using a relaxed molecular clock approach. We estimate the origin of nodes leading to extant members of the Arcellinida Order to have happened during the latest Mesoproterozoic and Neoproterozoic (1054 - 661 Ma), while the divergence of extant infraorders postdates the Silurian. Our results demonstrate that at least one major heterotrophic eukaryote lineage originated during the Neoproterozoic. A putative radiation of eukaryotic groups (e.g. Arcellinida) during the early-Neoproterozoic sustained by favorable ecological and environmental conditions may have contributed to eukaryotic life endurance during the Cryogenian severe ice ages. Moreover, we infer that Arcellinida most likely already inhabited terrestrial habitats during the Neoproterozoic, coexisting with terrestrial Fungi and green algae, before land plant radiation. The most recent extant Arcellinida groups diverged during the Silurian Period, alongside other taxa within Fungi and flowering plants. These findings shed light on heterotrophic microeukaryotes evolutionary history and ecological significance in Earths ecosystems, using testate amoebae as a proxy. Significance StatementArcellinida shelled amoebae are heterotrophic microbial eukaryotes with an extensive Neoproterozoic fossil record represented by the vase-shaped microfossils (VSMs), a diverse group that is abundant and widespread in late Tonian rocks (VSMs). Here we combined phylogenomic sampling and the fossil record to generate time-calibrated trees. Our results illuminate key events in the history of life, including: i) the Tonian origin of extant microbial eukaryote lineages; ii) a speculative proposed radiation of eukaryotes before the Cryogenian, "Tonian revolution"; iii) the establishment of complex terrestrial habitats before the Cryogenian; iv) a post-Silurian divergence of modern Arcellinida sub-clades in terrestrial (including freshwater) habitats. Our results provide valuable insights into the evolution of life throughout geological time and are congruent with recent discoveries regarding the early diversification of eukaryotes, including the Precambrian history of eukaryotic protosteroids.

evolutionary biology↗

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↗

Microeukaryotic predators shape the wastewater microbiome.

The physicochemical parameters that shape the prokaryotic community composition in wastewater have been extensively studied. In contrast, it is poorly understood whether and how biotic interactions affect the prokaryotic community composition in wastewater. We used metatranscriptomics data from a bioreactor sampled weekly over 14 months to investigate the wastewater microbiome, including often neglected microeukaryotes. Our analysis revealed that while prokaryotes are unaffected by seasonal changes in water temperature, they are impacted by a seasonal, temperature-induced change in the microeukaryotic community. Our findings suggest that selective predation pressure exerted by microeukaryotes is a significant factor shaping the prokaryotic community in wastewater. This study underscores the importance of investigating the entire wastewater microbiome to develop a comprehensive understanding of wastewater treatment.

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↗

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↗