Biocontrol Traits Correlate With Resistance to Predation by Protists in Soil Pseudomonads

Abstract

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.

Spatiotemporal Dynamics of Maize (Zea mays L.) Root Growth and Its Potential Consequences for the Assembly of the Rhizosphere Microbiota

“…There is increasing evidence that predator-prey dynamics of bacterivores contribute significantly to the deterministic processes that eventually determine microbiome composition and function (Rosenberg et al, 2009;Amacker et al, 2020;Rüger et al, 2021). Numbers of bacterivore protists show a steep increase toward the plant rhizosphere, where protist predation regulates bacterial turnover (Zwart et al, 1994;Alphei et al, 1996).…”

“…Few experiments to date studied how increased species richness of protistan predators feeds back on bacterial diversity and function. Single protist taxa differ in their feeding modes ( Glücksman et al, 2010 ; Flues et al, 2017 ; Amacker et al, 2020 ), and higher species richness was shown to strongly increase the exploitation of bacterial prey species ( Saleem et al, 2012 , 2013 ; Hünninghaus et al, 2017 ). It appears that protistan predation is enhancing bacterial biocontrol activity on roots ( Weidner et al, 2016 ; Xiong et al, 2018 ; Gao et al, 2019 ; Amacker et al, 2020 ).…”

“…A fundamental question for understanding plant-microbe relationships is where a predictable microbiome is formed along the root axis and through which microbial dynamics the stable formation of a microbiome is challenged. Theoretically, community assembly begins with random, unregulated colonization of taxa from nearby sites (i.e., neutral processes), a process that continues throughout the lifetime of roots; while ordered dynamics (microbiome assembly) occur through selection (i.e., niche-based processes) when (i) exudates promote fast-growing copiotrophic taxa, (ii) root signals attract specific symbionts or pathogens, (iii) increased competition due to limited resource availability leads to species sorting, and (iv) predation selects for specific microbial traits among members of the microbiome ( Vellend, 2010 ; Hardoim et al, 2011 ; Ho et al, 2017 ; Kudjordjie et al, 2019 ; Amacker et al, 2020 ; Chen et al, 2020 ). These microbial assembly processes again are embedded in plant-driven spatiotemporal dynamics at small and large scales, caused by differences in the quality and quantity of rhizodeposition: (i) along the root axis, (ii) during diurnal cycles, (iii) on different root types, and (iv) during plant development.…”

On the phenology of protists: Recurrent patterns reveal seasonal variation of protistan (Rhizaria: Cercozoa, Endomyxa) communities in tree canopies

“…bacterivorous protists (Mueller and Mueller 1970;Bamforth 1973Bamforth , 2007Bamforth , 2010Flues, Bass and Bonkowski 2017). Protistan predation has a profound influence on the structure and function of bacterial communities (Matz and Kjelleberg 2005;Krome et al 2010;Jousset 2012;Amacker et al 2020). Since these microbial eukaryotes comprise a vast array of functional traits in morphologies, locomotion and feeding modes (Fiore-Donno et al 2019;Dumack et al 2020), we presume that different protistan taxa play contrasting or complementary ecological roles within the heterogeneous habitat of forest canopy.…”

“…Protistan predation has a profound influence on the structure and function of bacterial communities (Matz and Kjelleberg 2005; Krome et al . 2010; Jousset 2012; Amacker et al . 2020).…”