Abstract
BackgroundPlant health is intimately influenced by the rhizosphere microbiome, a complex assembly of organisms that changes markedly across plant growth. However, most rhizosphere microbiome research has focused on fractions of this microbiome, particularly bacteria and fungi. It remains unknown how other microbial components, especially key microbiome predators—protists—are linked to plant health. Here, we investigated the holistic rhizosphere microbiome including bacteria, microbial eukaryotes (fungi and protists), as well as functional microbial metabolism genes. We investigated these communities and functional genes throughout the growth of tomato plants that either developed disease symptoms or remained healthy under field conditions.ResultsWe found that pathogen dynamics across plant growth is best predicted by protists. More specifically, communities of microbial-feeding phagotrophic protists differed between later healthy and diseased plants at plant establishment. The relative abundance of these phagotrophs negatively correlated with pathogen abundance across plant growth, suggesting that predator-prey interactions influence pathogen performance. Furthermore, phagotrophic protists likely shifted bacterial functioning by enhancing pathogen-suppressing secondary metabolite genes involved in mitigating pathogen success.ConclusionsWe illustrate the importance of protists as top-down controllers of microbiome functioning linked to plant health. We propose that a holistic microbiome perspective, including bacteria and protists, provides the optimal next step in predicting plant performance.4pRGo2biPz35arE7pbprXhVideo
Highlights
Plant health is intimately influenced by the rhizosphere microbiome, a complex assembly of organisms that changes markedly across plant growth
We found that the community structure of phagotrophic protists at plant establishment was indicative for later plant health, as indicated by the differences (ANOSIM, P = 0.013) observed between plants developing disease and those remaining healthy (Fig. 2a, b)
Phagotrophs and a phototrophic Chloroidium saccharophila were negatively linked with the pathogen at plant establishment (Fig. 2d). Those protistan operational taxonomic units (OTUs) were present in diseased plants, they did not correlate with the pathogen in the network analysis (Table S4)
Summary
Plant health is intimately influenced by the rhizosphere microbiome, a complex assembly of organisms that changes markedly across plant growth. Studies using model protists have shown that protists control microbiome diversity and structure leading to plant growth promotion [17, 18, 20] These changes are at least partly explained by the fact that protists feed selectively on microbial prey taxa, which differs between protistan species [21, 22]. Protists can, for instance, increase those bacteria that produce pathogen-suppressive secondary metabolites [23, 24] All these studies investigating potential links of protists with plant performance were carried out under artificial laboratory or greenhouse conditions focusing on one or few protistan species. We have yet to identify the links between a complex diversity of protists, the microbiome and plant performance, especially in agricultural systems under field conditions
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