Root-colonizing bacteria can support plant growth and help fend off pathogens. It is clear that such bacteria benefit from plant-derived carbon, but it remains ambiguous why they invest in plant-beneficial traits. We suggest that selection via protist predation contributes to recruitment of plant-beneficial traits in rhizosphere bacteria. To this end, we examined the extent to which bacterial traits associated with pathogen inhibition coincide with resistance to protist predation. We investigated the resistance to predation of a collection of Pseudomonas spp. against a range of representative soil protists covering three eukaryotic supergroups. We then examined whether patterns of resistance to predation could be explained by functional traits related to plant growth promotion, disease suppression and root colonization success. We observed a strong correlation between resistance to predation and phytopathogen inhibition. In addition, our analysis highlighted an important contribution of lytic enzymes and motility traits to resist predation by protists. We conclude that the widespread occurrence of plant-protective traits in the rhizosphere microbiome may be driven by the evolutionary pressure for resistance against predation by protists. Protists may therefore act as microbiome regulators promoting native bacteria involved in plant protection against diseases.
Predatory protists are major consumers of soil micro-organisms. By selectively feeding on their prey, they can shape soil microbiome composition and functions. While different protists are known to show diverging impacts, it remains impossible to predict a priori the effect of a given species. Various protist traits including phylogenetic distance, growth rate and volume have been previously linked to the predatory impact of protists. Closely-related protists,however, also showed distinct prey choices which could mirror specificity in their dietary niche. We, therefore, aimed to estimate the dietary niche breadth and overlap of eight protist isolates on 20 bacterial species in plate assays. To assess the informative value of previously suggested and newly proposed (feeding-related) protist traits, we related them to the impacts of predation of each protist on a protist-free soil bacterial community in a soil microcosm via 16S rRNA gene amplicon sequencing. We could demonstrate that each protist showed a distinct feeding pattern in vitro. Further, the assayed protist feeding patterns and growth rates correlated well with the observed predatory impacts on the structure of soil bacterial communities. We thus conclude that in vitro screening has the potential to inform on the specific predatory impact of selected protists.
An ever-increasing diversity of potentially toxic chemical compounds are being developed and released into the environment as a result of human activities (e.g. agriculture, drugs, and cosmetics). Among these, pesticides have been shown to affect non-targeted wildlife since the 1960s. A range of ecotoxicological tests are used to assess the toxicity of pesticides on various model organisms. However most model organisms are metazoans, while the majority of Eukaryotes are unicellular microorganisms known as protists. Protists are ubiquitous organisms of key functional roles in all ecosystems but are so far little studied with respect to pesticide impact. To fill this gap, we developed a new ecotoxicological test based on Euglypha rotunda, a common soil amoeba, grown in culture flask with Escherichia coli as sole food source. We tested this assay with the herbicide S-metolachlor, which is known to affect cell division in seedling shoots and roots of weeds. Reproducible growth conditions were obtained for E. rotunda. The growth of E. coli was not affected by the herbicide. The growth of E. rotunda was affected by the herbicide in a non-linear way, growth being significantly reduced at ca. 15 μg/L, but not at 150 μg/L. Our results show the potential for using soil protists in ecotoxicology and adds to the growing body of evidence for non-linear impacts of pesticides on non-target organisms. With the acquisition of additional data, the protocol should be suitable for standard ecotoxicological tests.
Protists are a paraphyletic group referring to all Eukaryotes except plants (Chloroplastida), animals (Metazoa) and Fungi (Figure 1; Burki et al. 2020). Soil protists are mostly unicellular and usually display a size range of few micrometers to millimeters (Geisen et al. 2017).As to be expected from their broad phylogenetic coverage (Figure 1), protists exhibit a huge variety of morphotypes with the classical division between amoebae, flagellates, ciliates and shell-forming (testate) types (Geisen et al. 2018;Burki et al. 2020). Including autotrophs, heterotrophs, mixotrophs and parasites, protists exhibit a range of ecological functions from primary producers to decomposers (Geisen et al. 2018). In the soil context, the major group is represented by heterotrophic, free-living protists (Figure 1; Oliverio et al. 2020; Singer et al. 2021; Xiong et al. 2021), which were traditionally referred to as "protozoa". Many heterotrophic protists are predators and feed on relatively small prey such as bacteria and yeast by ingesting them via phagocytosis, but others graze and/or attack bigger organisms such as hyphal-forming fungi, nematodes and other micro-eukaryotes (Geisen et al. 2015; Geisen 2016). Predatory impacts of protists on the bacterial communitiesIn their quality of predators, soil protists are mostly known for their role as main consumers of bacteria. As such, protists typically reduce the bacterial biomass (de Ruiter, Neutel, and Moore 1995; Clarholm 2005). Counterintuitively, however, the bacterivorous activity of protists is usually linked with an increase in microbial activity (Saleem and Moe 2014).This discrepancy is generally explained by the increased nutrient turnover that results from protist consumption (Sherr, Sherr, and Berman 1983;Clarholm 1984) as well as the removal of less active, senescent bacterial cells which are more likely to be preyed upon first. The removal of senescent cells lowers competition for space and makes nutrients available for the more active bacterial cells (Bonkowski 2004).Another crucial characteristic of protist consumption is prey selectivity (Montagnes et al. 2008). The protists can sense and discriminate between different prey based on size, shape and chemical properties including specific membrane-bound proteins but also volatiles compounds (VOCs) (Jousset 2012;Schulz-Bohm et al. 2017). Such prey discrimination and selectivity cause protists to modify bacterial community composition, favoring a specific subset of species (Bonkowski and Brandt 2002;Rønn et al. 2002). Noteworthy, distinct food preferences have been observed for phylogenetically closely related protists with similar morphotypes suggesting that each species has its own food preferences (Glücksman et al. 2010).In response to this predatory pressure, bacteria have evolved different escape and/ or defense strategies, including changes in bacterial cell morphology, colony formation, escaping movement and/or production of toxic compounds (Matz and Kjelleberg 2005).Numerous toxic compounds produced by soil Pseud...
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