Harnessing the potential of predatory protists to support a beneficial soil microbiome

Abstract

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...