Soil amoebae rapidly change bacterial community composition in the rhizosphere of Arabidopsis thaliana

Abstract

We constructed an experimental model system to study the effects of grazing by a common soil amoeba, Acanthamoeba castellanii, on the composition of bacterial communities in the rhizosphere of Arabidopsis thaliana. Amoebae showed distinct grazing preferences for specific bacterial taxa, which were rapidly replaced by grazing tolerant taxa in a highly reproducible way. The relative proportion of active bacteria increased although bacterial abundance was strongly decreased by amoebae. Specific bacterial taxa had disappeared already two days after inoculation of amoebae. The decrease in numbers was most pronounced in Betaproteobacteria and Firmicutes. In contrast, Actinobacteria, Nitrospira, Verrucomicrobia and Planctomycetes increased. Although other groups, such as betaproteobacterial ammonia oxidizers and Gammaproteobacteria did not change in abundance, denaturing gradient gel electrophoresis with specific primers for pseudomonads (Gammaproteobacteria) revealed both specific changes in community composition as well as shifts in functional genes (gacA) involved in bacterial defence responses. The resulting positive feedback on plant growth in the amoeba treatment confirms that bacterial grazers play a dominant role in structuring bacteria-plant interactions. This is the first detailed study documenting how rapidly protozoan grazers induce shifts in rhizosphere bacterial community composition.

Microbiology, Genomics, and Clinical Significance of the Pseudomonas fluorescens Species Complex, an Unappreciated Colonizer of Humans

“…The F113 strain was originally isolated from sugar beet rhizospheres in Ireland (158) and can inhibit the growth of plant-pathogenic bacteria, oomycetes, fungi, and a wide range of nematodes (159)(160)(161). Predation against protozoa in both terrestrial and aquatic environments is an important factor influencing bacterial community makeup and behavior (37,38,162). In F113, the SPI-I T3SS hilA promoter shows increased expression during close contact with the amoeba Acanthamoeba castellanii, suggesting that this T3SS is directly involved in protecting the bacterium from amoeba predation.…”

“…1), including soil, the rhizospheres and surfaces of plants, nonsterile pharmaceuticals, showerheads, and even indoor wall surfaces (23,24). P. fluorescens has been studied most widely as an environmental microbe, most notably for its role in promoting plant health via a number of encoded antimicrobial mechanisms (25)(26)(27)(28)(29)(30)(31)(32)(33)(34)(35)(36)(37)(38). However, P. fluorescens also possesses a number of functional traits that provide it with the capability to grow and thrive in mammalian hosts, including production of bioactive secondary metabolites (26-30, 33, 39-42), siderophores (43)(44)(45), and a type III secretion system (46)(47)(48)(49)(50)(51), the ability to form biofilms (20,(52)(53)(54)(55)(56), and the plasticity of some strains to adapt to growth at higher temperature (53,(57)(58)(59).…”

Diversity of protists and bacteria determines predation performance and stability

“…Bacteria are the main drivers of many biogeochemical cycles, nutrient recycling and trophic transfer of organic carbon and nitrogen (Falkowski et al, 2008). Similar to food web modules composed of larger organisms, topdown control by protistan predators regulates bacterial abundance, community composition and, consequently, has an influence on many microbial ecosystem processes (Simek et al, 1997;Pernthaler, 2005;Corno and Jü rgens, 2008;Rosenberg et al, 2009;Bell et al, 2010;Glü cksman et al, 2010). Although direct influences of top-down control of bacterial communities by protists have been studied earlier (for example, Bell et al, 2010;Roberts et al, 2011;Martinez-Garcia et al, 2012), relatively little is known about direct mutual effects of species richness on community structures and performances of the prey or predator communities, respectively.…”

Predator-Prey Chemical Warfare Determines the Expression of Biocontrol Genes by Rhizosphere-Associated Pseudomonas fluorescens

“…Bacterial communities are heavily consumed by protozoan predators (30), and predation is a major force shaping the structure of microbial communities in both aquatic and terrestrial ecosystems (34,35). The competitiveness of bacteria strongly depends on their ability to avoid predation (9,22), and many species have developed defense mechanisms such as the production of toxins, which reduces mortality by repelling or killing predators (21,24).…”