Protist communities are more sensitive to nitrogen fertilization than other microorganisms in diverse agricultural soils

Abstract

Background Agricultural food production is at the base of food and fodder, with fertilization having fundamentally and continuously increased crop yield over the last decades. The performance of crops is intimately tied to their microbiome as they together form holobionts. The importance of the microbiome for plant performance is, however, notoriously ignored in agricultural systems as fertilization disconnects the dependency of plants for often plant-beneficial microbial processes. Moreover, we lack a holistic understanding of how fertilization regimes affect the soil microbiome. Here, we examined the effect of a 2-year fertilization regime (no nitrogen fertilization control, nitrogen fertilization, and nitrogen fertilization plus straw amendment) on entire soil microbiomes (bacteria, fungi, and protist) in three common agricultural soil types cropped with maize in two seasons. Results We found that the application of nitrogen fertilizers more strongly affected protist than bacterial and fungal communities. Nitrogen fertilization indirectly reduced protist diversity through changing abiotic properties and bacterial and fungal communities which differed between soil types and sampling seasons. Nitrogen fertilizer plus straw amendment had greater effects on soil physicochemical properties and microbiome diversity than nitrogen addition alone. Moreover, nitrogen fertilization, even more together with straw, increased soil microbiome network complexity, suggesting that the application of nitrogen fertilizers tightened soil microbiomes interactions. Conclusions Together, our results suggest that protists are the most susceptible microbiome component to the application of nitrogen fertilizers. As protist communities also exhibit the strongest seasonal dynamics, they serve as the most sensitive bioindicators of soil changes. Changes in protist communities might have long-term effects if some of the key protist hubs that govern microbiome complexities as top microbiome predators are altered. This study serves as the stepping stone to promote protists as promising agents in targeted microbiome engineering to help in reducing the dependency on exogenous unsustainably high fertilization and pesticide applications. Electronic supplementary material The online version of this article (10.1186/s40168-019-0647-0) contains supplementary material, which is available to authorized users.

Combined Application of Organic and Inorganic Nitrogen Fertilizers Affects Soil Prokaryotic Communities Compositions

“…As well as biodiversity, the differences in the prokaryotic community compositions were significant among different treatments, which corresponded with previous research [38]. In our study, the top five dominant phyla across all samples were Proteobacteria, Acidobacteria, Chlorofexi, Actinobacteria, and Planctomycetes, which was similar to the results of two previous studies [35,49]. As the most abundant phyla of the soil bacteria, Proteobacteria, which were composed of gram-negative bacteria, preferred the environment with a high nutrient content demonstrated in the study of Byss [50].…”

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

“…Among protists, the most prevalent core taxa were all cercozoans from the phyla Filosa-Sarcomonadae and Filosa-Granofilosea affiliated to Allapsidae -Group Te (77% of samples), Limonofila borokensis (70%) and Paracercomonas (63%). These three taxa have also been identified as extremely common and abundant in the rhizosphere of Arabidopsis thaliana [38] and Allapsidae -Group Te as a hub taxon in the maize rhizosphere [39]. Five Oomycetes were also categorized as core taxa with three of them affiliated to the Pythium genus and one to Phytophthora that are both described as potential plant pathogens.…”

Rhizosphere protists are key determinants of plant health

“…Recently, it was shown that bacterial communities at plant establishment can predict plant health at maturity [26]. Yet, other microbial groups might be even better indicators to predict plant health, as for instance, protist communities were shown to respond more strongly to environmental inputs and vary more in their composition between seasons than bacteria and fungi [27].…”