Diurnal Rhythmicity in the Rhizosphere Microbiome-Mechanistic Insights and Significance for Rhizosphere Function

Abstract

The rhizosphere is a key interface between plants, microbes and the soil which influences plant health and nutrition and modulates terrestrial biogeochemical cycling. Recent research has shown that the rhizosphere environment is far more dynamic than previously recognised, with evidence emerging for diurnal rhythmicity in rhizosphere chemistry and microbial community composition. This rhythmicity is in part linked to the host plant's circadian rhythm, although some heterotrophic rhizosphere bacteria and fungi may also possess intrinsic rhythmicity. We review the evidence for diurnal rhythmicity in rhizosphere microbial communities and its link to the plant circadian clock. Factors which may drive microbial rhythmicity are discussed, including diurnal change in root exudate flux and composition, rhizosphere physico-chemical properties and plant immunity. Microbial processes which could contribute to community rhythmicity are considered, including self-sustained microbial rhythms, bacterial movement into and out of the rhizosphere, and microbe-microbe interactions. We also consider evidence that changes in microbial composition mediated by the plant circadian clock may affect microbial function and its significance for plant health and broader soil biogeochemical cycling processes. We identify key knowledge gaps and approaches which could help to resolve the spatial and temporal variation and functional significance of rhizosphere microbial rhythmicity. This includes unravelling the factors which determine the oscillation of microbial activity, growth and death, and cross-talk with the host over diurnal time frames. We conclude that diurnal rhythmicity is an inherent characteristic of the rhizosphere and that temporal factors should be considered and reported in rhizosphere studies.

Figure 1

The rhizosphere represents the roots and soil adjacent to roots. Root exudation drives growth of microbes in the rhizosphere and these communities can interact with the plant and soil to direct biogeochemical cycling processes, and plant health and nutrition. The plant and microbial communities exchange a range of signalling compounds which influence each other's growth and physiology.

Figure 2

Potential drivers of microbial rhythmicity in the plant rhizosphere. Changes linked to plant root exudation are highlighted in green and those linked to increased plant transpiration during the day are highlighted in blue. Rhythmically produced molecules with roles in plant defence or plant‐microbe interactions are shown in orange. Some rhizosphere bacteria and fungi may also possess a circadian clock which could directly control rhythmic growth and/or activity. [Color figure can be viewed at wileyonlinelibrary.com]

Figure 3

Key Knowledge gaps. Plant‐related questions are shown in grey bubbles and microbe‐related questions in yellow bubbles. [Color figure can be viewed at wileyonlinelibrary.com]