Contrasting protist communities (Cercozoa: Rhizaria) in pristine and earthworm-invaded North American deciduous forests

Earthworms are considered ecosystem engineers due to their fundamental impact on soil structure, soil processes and on other soil biota. An invasion of non-native earthworm species has altered soils of North America since European settlement, a process currently expanding into still earthworm-free forest ecosystems due to continuous spread and increasing soil temperatures owing to climate change. Although earthworms are known to modify soil microbial diversity and activity, it is as yet unclear how eukaryote consumers in soil microbial food webs will be affected. Here, we investigated how earthworm invasion affects the diversity of Cercozoa, one of the most dominant protist taxa in soils. Although the composition of the native cercozoan community clearly shifted in response to earthworm invasion, the communities of the different forests showed distinct responses. We identified 39 operational taxonomic units (OTUs) exclusively indicating earthworm invasion, hinting at an earthworm-associated community of Cercozoa. In particular, Woronina pythii, a hyper-parasite of plant-parasitic Oomycota in American forests, increased strongly in the presence of invasive earthworms, indicating an influence of invasive earthworms on oomycete communities and potentially on forest health, which requires further research.

Viral infections mediate microbial food web controls on the global carbon cycle under warming

Climate warming will likely disrupt the flow of matter and energy within ecosystems, threatening the global carbon balance. Microorganisms are fundamental components of carbon cycling and are thus integral to ecosystem climate responses. However, ecosystem responses to warming are uncertain due to the functional and trophic complexity of microbial food webs. Here, we expose two major black boxes hindering our ability to anticipate ecosystem climate responses: viral infection and predation by microbial predators. We review current knowledge and uncover critical gaps in knowledge about how warming will impact these important top-down controls on the global carbon cycle. Understanding and predicting ecosystem responses to climate change will require disentangling complex direct and indirect responses within microbial food webs.

Taxonomy and Phylogeny of the Dileptid Ciliate Genus Paradileptus (Protista: Ciliophora), With a Brief Review and Redescriptions of Two Species Isolated From a Wetland in Northern China

Members of the genus Paradileptus are apex predators in microbial food webs. They are often encountered in freshwater biotopes and have been used in research on water quality monitoring and ecology. Nevertheless, our understanding of the biodiversity of Paradileptus, especially its ecological and genetic diversities, is very poor which hinders our ability to understand the ecosystem services it provides. The present study gives a detailed account of two Chinese populations of Paradileptus elephantinus and P. conicus including their living morphology, infraciliature, and molecular phylogenies based on 18S, 5.8S, and ITS ribosomal DNA sequences. The phylogenetic relationships between these two species and other rhynchostomatians are investigated. We also explore the potential contribution of differentiation of the proboscis (e.g., extrusomes, dorsal brush, and differentiated kineties) to niche partitioning and speciation in Paradileptus. The global distribution of Paradileptus is summarized based on published data. Finally, a key to the identification of the valid species of Paradileptus is provided.

Heterotrophic Dinoflagellate Growth and Grazing Rates Reduced by Microplastic Ingestion

Microplastics are ubiquitous contaminants in marine ecosystems worldwide, threatening fisheries production, food safety, and human health. Ingestion of microplastics by fish and large zooplankton has been documented, but there are few studies focusing on single-celled marine predators, including heterotrophic dinoflagellates. In laboratory experiments, the heterotrophic dinoflagellate species Oxyrrhis marina and Gyrodinium sp. readily ingested both algal prey and polystyrene microplastic spheres (2.5–4.5 μm), while Protoperidinium sp. did not ingest microplastics. Compared to algae-only fed dinoflagellates, those that ingested microplastics had growth rates reduced by 25–35% over the course of 5 days. Reduced growth resulted in a 30–50% reduction of secondary production as measured as predator biomass. Ingestion rates of algal prey were also reduced in the microplastic treatments. When given a mixture of microplastics and algal prey, O. marina displayed a higher selectivity for algal prey than Gyrodinium sp. Observations in the coastal ocean showed that phylogenetically diverse taxa ingested microplastic beads, and thus heterotrophic dinoflagellates could contribute to trophic transfer of microplastics to higher trophic levels. The results of this study may suggest that continued increase in microplastic pollution in the ocean could lead to reduced secondary production of heterotrophic protists due to microplastic ingestion, altering the flow of energy and matter in marine microbial food webs.

Hydrodynamic interactions are key in thrust-generation of microswimmers with hairy flagella

The important role of flagellates in aquatic microbial food webs is mediated by their flagella that enable them to swim and generate a feeding current. The flagellum in most predatory flagellates is equipped with rigid hairs that reverse the direction of thrust compared to the thrust due to a smooth flagellum. Conventionally, such reversal has been attributed to drag anisotropy of individual hairs, neglecting their hydrodynamic interactions. Here, we show that hydrodynamic interactions are key to thrust-generation and reversal in hairy flagellates, making their hydrodynamics fundamentally different from the slender-body theory governing microswimmers with smooth flagella. Using computational fluid dynamics and model analysis, we demonstrate that long and not too closely spaced hairs and strongly curved flagellar waveforms are optimal for thrust-generation. Our results form a theoretical basis for understanding the diverse flagellar architectures and feeding modes found in predatory flagellates.

The Functional Significance of Bacterial Predators

ABSTRACT Predation structures food webs, influences energy flow, and alters rates and pathways of nutrient cycling through ecosystems, effects that are well documented for macroscopic predators. In the microbial world, predatory bacteria are common, yet little is known about their rates of growth and roles in energy flows through microbial food webs, in part because these are difficult to quantify. Here, we show that growth and carbon uptake were higher in predatory bacteria compared to nonpredatory bacteria, a finding across 15 sites, synthesizing 82 experiments and over 100,000 taxon-specific measurements of element flow into newly synthesized bacterial DNA. Obligate predatory bacteria grew 36% faster and assimilated carbon at rates 211% higher than nonpredatory bacteria. These differences were less pronounced for facultative predators (6% higher growth rates, 17% higher carbon assimilation rates), though high growth and carbon assimilation rates were observed for some facultative predators, such as members of the genera Lysobacter and Cytophaga, both capable of gliding motility and wolf-pack hunting behavior. Added carbon substrates disproportionately stimulated growth of obligate predators, with responses 63% higher than those of nonpredators for the Bdellovibrionales and 81% higher for the Vampirovibrionales, whereas responses of facultative predators to substrate addition were no different from those of nonpredators. This finding supports the ecological theory that higher productivity increases predator control of lower trophic levels. These findings also indicate that the functional significance of bacterial predators increases with energy flow and that predatory bacteria influence element flow through microbial food webs. IMPORTANCE The word “predator” may conjure images of leopards killing and eating impala on the African savannah or of great white sharks attacking elephant seals off the coast of California. But microorganisms are also predators, including bacteria that kill and eat other bacteria. While predatory bacteria have been found in many environments, it has been challenging to document their importance in nature. This study quantified the growth of predatory and nonpredatory bacteria in soils (and one stream) by tracking isotopically labeled substrates into newly synthesized DNA. Predatory bacteria were more active than nonpredators, and obligate predators, such as Bdellovibrionales and Vampirovibrionales, increased in growth rate in response to added substrates at the base of the food chain, strong evidence of trophic control. This work provides quantitative measures of predator activity and suggests that predatory bacteria—along with protists, nematodes, and phages—are active and important in microbial food webs.

Experimental identification and in silico prediction of bacterivory in green algae

While algal phago-mixotrophs play a major role in aquatic microbial food webs, their diversity remains poorly understood. Recent studies have indicated several species of prasinophytes, early diverging green algae, to be able to consume bacteria for nutrition. To further explore the occurrence of phago-mixotrophy in green algae, we conducted feeding experiments with live fluorescently labeled bacteria stained with CellTracker Green CMFDA, heat-killed bacteria stained with 5-(4,6-dichlorotriazin-2-yl) aminofluorescein (DTAF), and magnetic beads. Feeding was detected via microscopy and/or flow cytometry in five strains of prasinophytes when provided with live bacteria: Pterosperma cristatum NIES626, Pyramimonas parkeae CCMP726, Pyramimonas parkeae NIES254, Nephroselmis pyriformis RCC618, and Dolichomastix tenuilepis CCMP3274. No feeding was detected when heat-killed bacteria or magnetic beads were provided, suggesting a strong preference for live prey in the strains tested. In parallel to experimental assays, green algal bacterivory was investigated using a gene-based prediction model. The predictions agreed with the experimental results and suggested bacterivory potential in additional green algae. Our observations underline the likelihood of widespread occurrence of phago-mixotrophy among green algae, while additionally highlighting potential biases introduced when using prey proxy to evaluate bacterial ingestion by algal cells.

The Functional Significance of Bacterial Predators

Predation structures food webs, influences energy flow, and alters rates and pathways of nutrient cycling through ecosystems, effects that are well documented for macroscopic predators. In the microbial world, predatory bacteria are common, yet little is known about their rates of growth and roles in energy flows through microbial food webs, in part because these are difficult to quantify. Here, we show that growth and carbon uptake were higher in predatory bacteria compared to non-predatory bacteria, a finding across 15 sites, synthesizing 82 experiments and over 100,000 taxon-specific measurements of element flow into newly synthesized bacterial DNA. Obligate predatory bacteria grew 36% faster and assimilated carbon at rates 211% higher than non-predatory bacteria. These differences were less pronounced for facultative predators (6% higher growth rates, 17% higher carbon assimilation rates), though high growth and carbon assimilation rates were observed for some facultative predators, such as members of the genera Lysobacter and Cytophaga, both capable of gliding motility and wolfpack hunting behavior. Added carbon substrates disproportionately stimulated growth of obligate predators, with responses 63% higher than non-predators for the Bdellovibrionales and 81% higher for the Vampirovibrionales, whereas responses of facultative predators to substrate addition were no different from non-predators. This finding supports ecological theory that higher productivity increases predator control of lower trophic levels. These findings also indicate that the functional significance of bacterial predators increases with energy flow, and that predatory bacteria influence element flow through microbial food webs.

Taxonomic and Functional Diversity of Heterotrophic Protists (Cercozoa and Endomyxa) from Biological Soil Crusts

Biological soil crusts (biocrusts) accommodate diverse communities of phototrophic and heterotrophic microorganisms. Heterotrophic protists have critical roles in the microbial food webs of soils, with Cercozoa and Endomyxa often being dominant groups. Still, the diversity, community composition, and functions of Cercozoa and Endomyxa in biocrusts have been little explored. In this study, using a high-throughput sequencing method with taxon-specific barcoded primers, we studied cercozoan and endomyxan communities in biocrusts from two unique habitats (subarctic grassland and temperate dunes). The communities differed strongly, with the grassland and dunes being dominated by Sarcomonadea (69%) and Thecofilosea (43%), respectively. Endomyxa and Phytomyxea were the minor components in dunes. Sandonidae, Allapsidae, and Rhogostomidae were the most abundant taxa in both habitats. In terms of functionality, up to 69% of the grassland community was constituted by bacterivorous Cercozoa. In contrast, cercozoan and endomyxan communities in dunes consisted of 31% bacterivores, 25% omnivores, and 20% eukaryvores. Facultative and obligate eukaryvores mostly belonged to the families Rhogostomidae, Fiscullidae, Euglyphidae, Leptophryidae, and Cercomonadidae, most of which are known to feed mainly on algae. Biocrust edaphic parameters such as pH, total organic carbon, nitrogen, and phosphorus did not have any significant influence on shaping cercozoan communities within each habitat, which confirms previous results from dunes.