RESUMO
Heterotrophic protists are vital in Earth's 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 to 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 Earth's ecosystems, using testate amoebae as a proxy.
Assuntos
Ecossistema , Fósseis , Processos Heterotróficos , Filogenia , Biodiversidade , Evolução Biológica , Amebozoários/genética , Amebozoários/classificação , Amoeba/genética , Amoeba/classificação , Amoeba/fisiologia , Eucariotos/genética , Eucariotos/classificaçãoRESUMO
Protists, a crucial part of the soil food web, are increasingly acknowledged as significant influencers of nutrient cycling and plant performance in farmlands. While topographical and climatic factors are often considered to drive microbial communities on a continental scale, higher trophic levels like heterotrophic protists also rely on their food sources. In this context, bacterivores have received more attention than fungivores. Our study explored the connection between the community composition of protists (specifically Rhizaria and Cercozoa) and fungi across 156 cereal fields in Europe, spanning a latitudinal gradient of 3000 km. We employed a machine-learning approach to measure the significance of fungal communities in comparison to bacterial communities, soil abiotic factors, and climate as determinants of the Cercozoa community composition. Our findings indicate that climatic variables and fungal communities are the primary drivers of cercozoan communities, accounting for 70% of their community composition. Structural equation modelling (SEM) unveiled indirect climatic effects on the cercozoan communities through a change in the composition of the fungal communities. Our data also imply that fungivory might be more prevalent among protists than generally believed. This study uncovers a hidden facet of the soil food web, suggesting that the benefits of microbial diversity could be more effectively integrated into sustainable agriculture practices.
Assuntos
Grão Comestível , Fungos , Microbiologia do Solo , Fungos/classificação , Fungos/genética , Fungos/isolamento & purificação , Europa (Continente) , Grão Comestível/microbiologia , Solo/química , Cercozoários , Bactérias/classificação , Bactérias/genética , Bactérias/isolamento & purificação , Cadeia Alimentar , Microbiota , Biodiversidade , Micobioma , AgriculturaRESUMO
The importance of host-associated microorganisms and their biotic interactions for plant health and performance has been increasingly acknowledged. Protists, main predators and regulators of bacteria and fungi, are abundant and ubiquitous eukaryotes in terrestrial ecosystems. Protists are considered to benefit plant health and performance, but the community structure and functions of plant-associated protists remain surprisingly underexplored. Harnessing plant-associated protists and other microbes can potentially enhance plant health and productivity and sustain healthy food and agriculture systems. In this review, we summarize the knowledge of multifunctionality of protists and their interactions with other microbes in plant hosts, and propose a future framework to study plant-associated protists and utilize protists as agrifood tools for benefiting agricultural production.
Assuntos
Ecossistema , Eucariotos , Plantas , Fungos/genética , Agricultura , Microbiologia do SoloRESUMO
Protists are abundant, diverse and perform essential functions in soils. Protistan community structure and its change across time or space are traditionally studied at the species level but the relative importance of the processes shaping these patterns depends on the taxon phylogenetic resolution. Using 18S rDNA amplicon data of the Cercozoa, a group of dominant soil protists, from an agricultural field in western Germany, we observed a turnover of relatively closely related taxa (from sequence variants to genus-level clades) across soil depth; while across soil habitats (rhizosphere, bulk soil, drilosphere), we observed turnover of relatively distantly related taxa, confirming Paracercomonadidae as a rhizosphere-associated clade. We extended our approach to show that closely related Cercozoa encounter divergent arbuscular mycorrhizal (AM) fungi across soil depth and that distantly related Cercozoa encounter closely related AM fungi across soil compartments. This study suggests that soil Cercozoa community assembly at the field scale is driven by niche-based processes shaped by evolutionary legacy of adaptation to conditions primarily related to the soil compartment, followed by the soil layer, giving a deeper understanding on the selection pressures that shaped their evolution.
Assuntos
Cercozoários , Micorrizas , Solo/química , Filogenia , Microbiologia do Solo , Rizosfera , Micorrizas/genéticaRESUMO
Hermesinum adriaticum is a rare marine and brackish flagellate that is of considerable interest due to its markable and fossilizable siliceous skeleton. Based on this skeleton, Hermesinum was initially considered a microalga of the Dictyochophyceae (Ochrophyta, Stramenopiles). Later on, it was assigned to the Ebriida due to its similarity to Ebria tripartita. The taxonomic assignment of the Ebriida, however, changed several times until it was placed within the Thecofilosea (Cercozoa, Rhizaria), based on genetic data of E. tripartita. We sequenced the 18S marker gene sequence of Hermesinum and confirm the close relationship of Ebria and Hermesinum.
Assuntos
Cercozoários , Rhizaria , Cercozoários/genética , Filogenia , Rhizaria/genéticaRESUMO
The majority of Euglyphida species are characterised by shells with imbricated silica scales. Environmental surveys indicate a large unexplored diversity and recent efforts hinted at a certain diversity of yet undescribed, inconspicuous, scale-lacking Euglyphida. Here we describe Phaeobola aeris gen. nov., sp. nov. that shows a variety of morphological characters typical for the Euglyphida but lacks silica scales-instead, this species bears an agglutinated test. Neither its morphology nor phylogenetic placement allows its assignment to any currently described family. We erected the yet monospecific genus Phaeobola gen. nov., which with yet available data remain Euglyphida incertae sedis.
Assuntos
Cercozoários , Rhizaria , Ursidae , Animais , FilogeniaRESUMO
Thecofilosea is a class in Cercozoa (Rhizaria) comprising mainly freshwater-inhabiting algivores. Recently, numerous isolates of thecofilosean amoebae have been cultured and were characterized by an integrated morphological and molecular approach. As attempts to establish a culture of Lecythium mutabilis repeatedly failed, it was not yet investigated by molecular means. We isolated single cells of L. mutabilis directly from their habitat and successfully sequenced the V4 region of their SSU rDNA. Phylogenetic analyses showed that L. mutabilis is not directly related to the genus Lecythium and instead branches within the Fiscullidae (Tectofilosida, Thecofilosea). Accordingly, we transfer the species L. mutabilis to a novel genus Omnivora gen. nov.
Assuntos
Cercozoários/classificação , Cercozoários/citologia , Cercozoários/genética , DNA de Protozoário/análise , DNA Ribossômico/análise , FilogeniaRESUMO
Thecofilosea is a class in Cercozoa comprising mainly freshwater inhabiting algivores. Since direct observation of amoeboid protists in soil is not possible, the prey spectra of their terrestrial relatives remain obscure. To test for grazing selectivity and the preferred prey of terrestrial thecofiloseans, we conducted a food choice experiment including yeasts and algae as prey. When being offered all food sources at once, the yeast cells were strongly reduced, whereas the abundance of the algae only slightly decreased. Since Fisculla terrestris thrives with fungal prey, it must be considered as a predator of eukaryotes with high preference for fungal cells.
Assuntos
Cercozoários/fisiologia , Cadeia Alimentar , Fungos , HerbivoriaRESUMO
A major drawback in testate amoeba research is a general lack of scientific studies combining molecular approaches and classical laboratory experiments. We isolated five yet uncultured testate amoebae of the genus Phryganella Penard, 1902 from three different rivers and one pond in Germany. Based on established cultures we show their morphology, which we studied by light and electron microscopy, and present their unique feeding mode on abundant and common pennate diatoms like Nitzschia spp. and Synedra spp., whose frustules are bent and frequently, but not always, broken during the feeding process. We further obtained the first SSU rDNA sequences of strains of the family Phryganellidae, all of which contain introns. We used the sequences to confirm the taxonomic placement of the Phryganellidae in the Arcellinida (Amoebozoa), branching as a sister group to the Cryptodifflugiidae.
Assuntos
Amebozoários/fisiologia , Cadeia Alimentar , Amebozoários/genética , DNA de Protozoário/análise , DNA Ribossômico/análise , Diatomáceas , Comportamento Alimentar , Água Doce , Alemanha , Características de História de Vida , Microscopia , Microscopia Eletrônica de VarreduraRESUMO
Despite their importance, how plant communities and soil microorganisms interact to determine the capacity of ecosystems to provide multiple functions simultaneously (multifunctionality) under climate change is poorly known. We conducted a common garden experiment using grassland species to evaluate how plant functional structure and soil microbial (bacteria and protists) diversity and abundance regulate soil multifunctionality responses to joint changes in plant species richness (one, three and six species) and simulated climate change (3°C warming and 35% rainfall reduction). The effects of species richness and climate on soil multifunctionality were indirectly driven via changes in plant functional structure and their relationships with the abundance and diversity of soil bacteria and protists. More specifically, warming selected for the larger and most productive plant species, increasing the average size within communities and leading to reductions in functional plant diversity. These changes increased the total abundance of bacteria that, in turn, increased that of protists, ultimately promoting soil multifunctionality. Our work suggests that cascading effects between plant functional traits and the abundance of multitrophic soil organisms largely regulate the response of soil multifunctionality to simulated climate change, and ultimately provides novel experimental insights into the mechanisms underlying the effects of biodiversity and climate change on ecosystem functioning.
Assuntos
Mudança Climática , Fenômenos Fisiológicos Vegetais , Microbiologia do Solo , Solo , Fenômenos Fisiológicos Bacterianos , Biodiversidade , Ecossistema , Solo/químicaRESUMO
The genus Diaphoropodon, Archer 1869, comprises filose amoebae with agglutinated tests made of quartz grains, diatom frustules and other particulate materials. The key trait of the genus is a hyaline theca covered with numerous 5- to 10-µm-long, hairlike rods. Based on SSU rDNA phylogeny, we show that Diaphoropodon groups closely to Lecythium, a testate amoeba genus with a flexible but naked theca. Electron microscopic images reveal that the rods of Diaphoropodon are not perforating the test but lie randomly distributed on the surface of the amoeba. Comparing fairly naked cells from our cultures with cells from the environment leads to the conclusion that these rods play a role in agglutinating the material on the test.
Assuntos
Amoeba/classificação , Agregação Celular/fisiologia , Cercozoários/classificação , Amoeba/genética , Cercozoários/genética , DNA de Protozoário/genética , DNA Ribossômico/genética , Microscopia Eletrônica , Filogenia , Reação em Cadeia da PolimeraseRESUMO
Cercomonads are among the most abundant and diverse groups of heterotrophic flagellates in terrestrial systems and show an affinity to plants. However, we still lack basic knowledge of plant-associated protists. We isolated 75 Cercomonadida strains from the phyllosphere and rhizosphere of plants from three functional groups: grasses (Poa sp.), legumes (Trifolium sp.) and forbs (Plantago sp.), representing 28 OTUs from the genera Cercomonas, Neocercomonas and Paracercomonas. The community composition differed clearly between phyllosphere and rhizosphere, but was not influenced by plant species identity. From these isolates we describe three novel cercomonad species including Neocercomonas epiphylla that was consistently and exclusively isolated from the phyllosphere. For each new species we provide a detailed morphological description as well as an 18S rDNA gene sequence as a distinct marker of species identity. Our data contribute to a better resolution of the systematics of cercomonads and their association with plants, by describing three novel species and adding gene sequences of 10 new cercomonad genotypes and of nine previously described species. In view of the functional importance of cercozoan communities in the phyllosphere and rhizosphere of plants, a more detailed understanding of their composition, function and predator-prey interactions are clearly required.
Assuntos
Biodiversidade , Cercozoários/isolamento & purificação , Folhas de Planta/parasitologia , Solo/parasitologia , Cercozoários/classificação , Cercozoários/genética , Cercozoários/crescimento & desenvolvimento , Filogenia , Plantago/parasitologia , Poa/parasitologia , Rizosfera , Trifolium/parasitologiaRESUMO
Invasive earthworms colonize ecosystems around the globe. Compared to other species' invasions, earthworm invasions have received little attention. Previous studies indicated their tremendous effects on resident soil biota representing a major part of the terrestrial biodiversity. We investigated effects of earthworm invasion on soil microbial communities in three forests in North America by conducting DNA sequencing of soil bacteria, fungi, and protists in two soil depths. Our study shows that microbial diversity was lower in highly invaded forest areas. While bacterial diversity was strongly affected compared to fungi and protists, fungal community composition and family dominance were strongly affected compared to bacteria and protists. We found most species specialized on invasion in fungi, mainly represented by saprotrophs. Comparably, few protist species, mostly bacterivorous, were specialized on invasion. As one of the first observational studies, we investigated earthworm invasion on three kingdoms showing distinct taxa- and trophic level-specific responses to earthworm invasion.
RESUMO
Understanding the environmental and biological mechanisms shaping latitudinal patterns in microbial diversity is challenging in the field of ecology. Although multiple hypotheses have been proposed to explain these patterns, a consensus has rarely been reached. Here, we conducted a large-scale field survey and microcosm experiments to investigate how environmental heterogeneity and putative trophic interactions (exerted by protist-bacteria associations and T4-like virus-bacteria associations) affect soil bacterial communities along a latitudinal gradient. We found that the microbial latitudinal diversity was kingdom dependent, showing decreasing, clumped, and increasing trends in bacteria, protists, and T4-like viruses, respectively. Climatic and edaphic drivers played predominant roles in structuring the bacterial communities; the intensity of the climatic effect increased sharply from 30°N to 32°N, whereas the intensity of the edaphic effect remained stable. Biotic associations were also essential in shaping the bacterial communities, with protist-bacteria associations showing a quadratic distribution, whereas virus-bacteria associations were significant only at high latitudes. The microcosm experiments further revealed that the temperature component, which is affiliated with climate conditions, is the primary regulator of trophic associations along the latitudinal gradient. Overall, our study highlights a previously underestimated mechanism of how the putative biotic interactions influence bacterial communities and their response to environmental gradients.
Assuntos
Bactérias , Microbiologia do Solo , Temperatura , Bactérias/classificação , Bactérias/genética , Bactérias/isolamento & purificação , Biodiversidade , Eucariotos , MicrobiotaRESUMO
The shells of testate amoebae are morphologically diverse and persistent in the environment. Accordingly, the examination of the morphology and composition of shells became a standard tool in ecological, palaeoecological, and evolutionary studies. However, so far the function of the shell remains poorly understood and, although based on limited evidence, the shell was considered as a defense mechanism. Based on recent evidence, we propose that the shell of arcellinid testate amoebae is a crucial component facilitating the amoebae's attack of large prey. Accordingly, the shell is not purely protective, but must be considered also as a weapon. This change in perspective opens up numerous new avenues in protistology and will lead to a substantial change in ecological, palaeoecological, and evolutionary research.
Assuntos
Amoeba , Lobosea , Filogenia , Evolução BiológicaRESUMO
Biological nitrogen fixation by free-living bacteria and rhizobial symbiosis with legumes plays a key role in sustainable crop production. Here, we study how different crop combinations influence the interaction between peanut plants and their rhizosphere microbiota via metabolite deposition and functional responses of free-living and symbiotic nitrogen-fixing bacteria. Based on a long-term (8 year) diversified cropping field experiment, we find that peanut co-cultured with maize and oilseed rape lead to specific changes in peanut rhizosphere metabolite profiles and bacterial functions and nodulation. Flavonoids and coumarins accumulate due to the activation of phenylpropanoid biosynthesis pathways in peanuts. These changes enhance the growth and nitrogen fixation activity of free-living bacterial isolates, and root nodulation by symbiotic Bradyrhizobium isolates. Peanut plant root metabolites interact with Bradyrhizobium isolates contributing to initiate nodulation. Our findings demonstrate that tailored intercropping could be used to improve soil nitrogen availability through changes in the rhizosphere microbiome and its functions.
Assuntos
Fabaceae , Fixação de Nitrogênio , Fabaceae/microbiologia , Nodulação , Solo , Microbiologia do Solo , Simbiose , Arachis , Verduras , Nitrogênio , Nódulos Radiculares de Plantas/microbiologiaRESUMO
Organismal functional strategies form a continuum from slow- to fast-growing organisms, in response to common drivers such as resource availability and disturbance. However, whether there is synchronisation of these strategies at the entire community level is unclear. Here, we combine trait data for >2800 above- and belowground taxa from 14 trophic guilds spanning a disturbance and resource availability gradient in German grasslands. The results indicate that 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. Using 15 indicators of carbon and nutrient fluxes, biomass production and decomposition, we also show that fast trait communities are associated with faster rates of ecosystem functioning. These findings demonstrate that 'slow' and 'fast' strategies can be manifested at the level of whole communities, opening new avenues of ecosystem-level functional classification.
Assuntos
Biodiversidade , Ecossistema , Biomassa , Agricultura , SoloRESUMO
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.
Assuntos
Microbiota , Águas Residuárias , ÁguaRESUMO
Understanding how antibiotic resistance emerges and evolves in natural habitats is critical for predicting and mitigating antibiotic resistance in the context of global change. Bacteria have evolved antibiotic production as a strategy to fight competitors, predators and other stressors, but how predation pressure of their most important consumers (i.e., protists) affects soil antibiotic resistance genes (ARGs) profiles is still poorly understood. To address this gap, we investigated responses of soil resistome to varying levels of protistan predation by inoculating low, medium and high concentrations of indigenous soil protist suspensions in soil microcosms. We found that an increase in protistan predation pressure was strongly associated with higher abundance and diversity of soil ARGs. High protist concentrations significantly enhanced the abundances of ARGs encoding multidrug (oprJ and ttgB genes) and tetracycline (tetV) efflux pump by 608%, 724% and 3052%, respectively. Additionally, we observed an increase in the abundance of numerous bacterial genera under high protistan pressure. Our findings provide empirical evidence that protistan predation significantly promotes antibiotic resistance in soil bacterial communities and advances our understanding of the biological driving forces behind the evolution and development of environmental antibiotic resistance.
Assuntos
Genes Bacterianos , Solo , Animais , Comportamento Predatório , Microbiologia do Solo , Bactérias/genética , Antibacterianos/farmacologia , Resistência Microbiana a Medicamentos/genética , Eucariotos/genéticaRESUMO
Arcellinida is ascending in importance in protistology, but description of their diversity still presents multiple challenges. Furthermore, applicable tools for surveillance of these organisms are still in developing stages. Importantly, a good database that sets a correspondence between molecular barcodes and species morphology is lacking. Cytochrome oxidase (COI) has been suggested as the most relevant marker for species discrimination in Arcellinida. However, some major groups of Arcellinida are still lacking a COI sequence. Here we expand the database of COI marker sequences for Arcellinids, using single-cell PCR, transcriptomics, and database scavenging. In the present work, we added 24 new Arcellinida COI sequences to the database, covering all unsampled infra- and suborders. Additionally, we added six new SSUrRNA sequences and described four new species using morphological, morphometrical, and molecular evidence: Heleopera steppica, Centropyxis blatta, Arcella uspiensis, and Cylindrifflugia periurbana. This new database will provide a new starting point to address new research questions from shell evolution, biogeography, and systematics of arcellinids.