Protists: Puppet Masters of the Rhizosphere Microbiome

Abstract

The rhizosphere microbiome is a central determinant of plant performance. Microbiome assembly has traditionally been investigated from a bottom-up perspective, assessing how resources such as root exudates drive microbiome assembly. However, the importance of predation as a driver of microbiome structure has to date largely remained overlooked. Here we review the importance of protists, a paraphyletic group of unicellular eukaryotes, as a key regulator of microbiome assembly. Protists can promote plant-beneficial functions within the microbiome, accelerate nutrient cycling, and remove pathogens. We conclude that protists form an essential component of the rhizosphere microbiome and that accounting for predator-prey interactions would greatly improve our ability to predict and manage microbiome function at the service of plant growth and health.A Multitrophic Perspective on the Rhizosphere Microbiome Plant growth, nutrition, and health are to a large extent determined by the activity of associated microorganisms [1]. In particular, plant roots are associated with an active multispecies community, the rhizosphere microbiome (see Glossary), providing several important services to the plant. Root-associated microbes, for instance, mineralize nutrients, manipulate plant hormonal balance, and suppress potential pathogens [2]. The species composition of the rhizosphere microbiome is now recognized to have direct effects on host plant traits [3]. However, our understanding of the determinants of microbiome community assembly and composition is still lacunar, restricting our ability to predict and harness microbiome dynamics and functionality. To date, most studies seeking to address the mechanisms underlying microbiome composition, species turnover, and function have focused on bottom-up drivers of microbial community composition, such as plant developmental stage, soil type, and host genotype [4][5][6]. While bottom-up control is certainly crucial, it represents only half of the story (Figure 1). Microorganisms in the rhizosphere are subjected to top-down control by a range of bacterial and eukaryotic consumers. Among them, free-living protists (Box 1), a highly diverse group of mostly unicellular eukaryotes [7], in our opinion deserve special attention. Protists are highly abundant and active consumers of bacteria and arguably fungi, impact community structure, and play a key role for nutrient cycling in the rhizosphere [8][9][10][11][12][13]. This review primarily addresses the importance of free-living, heterotrophic protists that feed on other organisms. For the sake of simplicity, we hereafter refer to them as 'protists', deliberately omitting mutualistic or parasitic taxa, including animal parasites or plant pathogens.

Influence of plant genotype and soil on the wheat rhizosphere microbiome: Evidences for a core microbiome across eight African and European soils

“…These observations are consistent with previous plant microbiome studies considering oomycetes diversity, that always described Pythium as the most dominant taxa among oomycetes [38,40,41]. These results confirm that protists are an integral part of the plant holobiont and their roles in controlling microbial populations through predation, disease incidence or contribution to nutrient cycles through the microbial loop deserve more attention [13].…”

“…amoeba, ciliates, stramenopiles) is currently available. Protists as predators, saprotrophs or phototrophs influence nutrient cycles in the rhizosphere and exert a strong top-down control on microbial (mainly bacterial) biomass and composition [13]. Still, despite protists high diversity and biomass in the rhizosphere, they represent an overlooked component of the plant holobiont.…”

Comparative Analysis of Rhizosphere Microbiomes of Southern Highbush Blueberry (Vaccinium corymbosum L.), Darrow’s Blueberry (V. darrowii Camp), and Rabbiteye Blueberry (V. virgatum Aiton)

“…The co-occurrence analysis of bacteria, fungi, and protozoa revealed complex networks with numerous positive and negative correlations, similar to those described in the rhizosphere of wild and managed V. angustifolium (Yurgel et al, 2018). Interestingly, our analysis also revealed that microbial communities of SHB, Vd, and Vg differ in the abundance of various predatory protists, which feed on bacteria and fungi and have recently emerged as a key factor that shapes the rhizosphere microbiome and selects for plant-beneficial functional traits (Gao et al, 2019).…”

Rhizosphere protists are key determinants of plant health

“…However, pathogen success and plant health are ultimately controlled by other biota, particularly the rhizosphere microbiome [3,4]. The plant rhizosphere microbiome is a complex assembly of diverse microorganisms, including bacteria, fungi, and protists that together influence plant health [5][6][7][8]. Despite the fact that the microbiome consists of diverse groups, most research aiming to understand the role of the microbiome in plant health or disease suppression has focused on bacteria [9][10][11] and fungi [12,13].…”