ABSTRACT Specific interactions between bacteria and ectomycorrhizal fungi (EcMF) can benefit plant health, and saprotrophic soil fungi represent a potentially antagonistic guild to these mutualisms. Yet there is little field‐derived experimental evidence showing how the relationship among these three organismal groups manifests across time. To bridge this knowledge gap, we experimentally reduced EcMF in forest soils and monitored both bacterial and fungal soil communities over the course of a year. Our analyses demonstrate that soil trenching shifts the community composition of fungal communities towards a greater abundance of taxa with saprotrophic traits, and this shift is linked to a decrease in both EcMF and a common ectomycorrhizal helper bacterial genus,Burkholderia, in a time‐dependent manner. These results not only reveal the temporal nature of a widespread tripartite symbiosis between bacteria, EcMF and a shared host tree, but they also refine our understanding of the commonly referenced ‘Gadgil effect’ by illustrating the cascading effects of EcMF suppression and implicating soil saprotrophic fungi as potential antagonists on bacterial‐EcMF interactions. 
                        more » 
                        « less   
                    
                            
                            Ectomycorrhizal fungi alter soil food webs and the functional potential of bacterial communities
                        
                    
    
            ABSTRACT Most of Earth’s trees rely on critical soil nutrients that ectomycorrhizal fungi (EcMF) liberate and provide, and all of Earth’s land plants associate with bacteria that help them survive in nature. Yet, our understanding of how the presence of EcMF modifies soil bacterial communities, soil food webs, and root chemistry requires direct experimental evidence to comprehend the effects that EcMF may generate in the belowground plant microbiome. To this end, we grewPinus muricataplants in soils that were either inoculated with EcMF and native forest bacterial communities or only native bacterial communities. We then profiled the soil bacterial communities, applied metabolomics and lipidomics, and linked omics data sets to understand how the presence of EcMF modifies belowground biogeochemistry, bacterial community structure, and their functional potential. We found that the presence of EcMF (i) enriches soil bacteria linked to enhanced plant growth in nature, (ii) alters the quantity and composition of lipid and non-lipid soil metabolites, and (iii) modifies plant root chemistry toward pathogen suppression, enzymatic conservation, and reactive oxygen species scavenging. Using this multi-omic approach, we therefore show that this widespread fungal symbiosis may be a common factor for structuring soil food webs.IMPORTANCEUnderstanding how soil microbes interact with one another and their host plant will help us combat the negative effects that climate change has on terrestrial ecosystems. Unfortunately, we lack a clear understanding of how the presence of ectomycorrhizal fungi (EcMF)—one of the most dominant soil microbial groups on Earth—shapes belowground organic resources and the composition of bacterial communities. To address this knowledge gap, we profiled lipid and non-lipid metabolites in soils and plant roots, characterized soil bacterial communities, and compared soils amended either with or without EcMF. Our results show that the presence of EcMF changes soil organic resource availability, impacts the proliferation of different bacterial communities (in terms of both type and potential function), and primes plant root chemistry for pathogen suppression and energy conservation. Our findings therefore provide much-needed insight into how two of the most dominant soil microbial groups interact with one another and with their host plant. 
        more » 
        « less   
        
    
    
                            - PAR ID:
- 10513361
- Editor(s):
- Gao, Cheng
- Publisher / Repository:
- American Society for Microbiology
- Date Published:
- Journal Name:
- mSystems
- ISSN:
- 2379-5077
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
- 
            
- 
            Abstract Efforts to catalog global biodiversity have often focused on aboveground taxonomic diversity, with limited consideration of belowground communities. However, diversity aboveground may influence the diversity of belowground communities and vice versa. In addition to taxonomic diversity, the structural diversity of plant communities may be related to the diversity of soil bacterial and fungal communities, which drive important ecosystem processes but are difficult to characterize across broad spatial scales. In forests, canopy structural diversity may influence soil microorganisms through its effects on ecosystem productivity and root architecture, and via associations between canopy structure, stand age, and species richness. Given that structural diversity is one of the few types of diversity that can be readily measured remotely (e.g., using light detection and ranging—LiDAR), establishing links between structural and microbial diversity could facilitate the detection of belowground biodiversity hotspots. We investigated the potential for using remotely sensed information about forest structural diversity as a predictor of soil microbial community richness and composition. We calculated LiDAR‐derived metrics of structural diversity as well as a suite of stand and soil properties from 38 forested plots across the central hardwoods region of Indiana, USA, to test whether forest canopy structure is linked with the community richness and diversity of four key soil microbial groups: bacteria, fungi, arbuscular mycorrhizal (AM) fungi, and ectomycorrhizal (EM) fungi. We found that the density of canopy vegetation is positively associated with the taxonomic richness (alpha diversity) of EM fungi, independent of changes in plant taxonomic richness. Further, structural diversity metrics were significantly correlated with the overall community composition of bacteria, EM, and total fungal communities. However, soil properties were the strongest predictors of variation in the taxonomic richness and community composition of microbial communities in comparison with structural diversity and tree species diversity. As remote sensing tools and algorithms are rapidly advancing, these results may have important implications for the use of remote sensing of vegetation structural diversity for management and restoration practices aimed at preserving belowground biodiversity.more » « less
- 
            Abstract Background and aimsPlant interactions with soil microbial communities are critical for understanding plant health, improving horticultural and agricultural outcomes, and maintaining diverse natural communities. In some cases, disease suppressive soils enhance plant survival in the presence of pathogens. However, species-specific differences and seasonal variation complicate our understanding of the drivers of soil fungal communities and their consequences for plants. Here, we aim to describe soil fungal communities acrossRhododendronspecies and seasons as well as the test for fungal indicators ofRhododendronspecies in the soil. Further, we test possible mechanisms governing disease suppressive soils to the oomycete pathogenPhytophthora cinnamomi. Variation in disease susceptibility to this pathogen across species and clades allows us to test for possible fungal drivers of disease suppressive soils. MethodsWe conducted high throughput sequencing of the fungal communities found in soil collected under 14Rhododendronspecies and across 2 seasons (April, October) at two sites in Ohio, USA. Phylogenetic analyses were used to ask whether fungal community composition correlated with increased plant survival with the addition of whole soil communities from a prior greenhouse experiment. ResultsEffects ofRhododendronspecies (R2 = 0.13), season (R2 = 0.01) and their interaction on fungal communities (R2 = 0.11) were statistically significant. Fungal community composition negatively correlated with survival following exposure to whole soil microbial communities, though this result depended on the presence ofR. minus. Forty-fiveTrichodermataxa were identified across our soil samples, and someTrichodermawere significantly associated with particularRhododendronspecies (e.g.Trichoderma atroviridewas associated withR. molle) in indicator species analyses. ConclusionThe correlation between plant responses to soil biotic communities and fungal community composition, as well as the presence of potential beneficial taxa such asTrichodermaand mycorrhizal fungi, are consistent with fungal-mediated survival benefits from the pathogenPhytophthora cinnamomi.more » « less
- 
            Background and Aims The soil-borne pathogen Phytophthora cinnamomi causes a deadly plant disease. Phosphite is widely used as an effective treatment to protect plants from Phytophthora cinnamomi. Phosphite as a common fungicide might influence the composition of soil fungal communities. However, whether the belowground effects of phosphitemediated protections are direct or indirectly mediated through soil biota are unknown. Therefore, exploring belowground effects could contribute to the evaluation of the sustainability of phosphite use and tests hypotheses about direct versus indirect effects in pathogen response. Methods Our greenhouse pot experiment on Rhododendron species had either an after-pathogen or a before-pathogen use of phosphite to compare and evaluate plant and soil fungal responses to phosphite and the presence of an oomycete pathogen Phytophthora cinnamomi. The factorial experiment also included with and without pathogen and soil biota treatments, for a test of interactive effects. High throughput sequencing analyzed the soil fungal communities, and we measured the diversity, evenness and richness of soil fungi. Results Phosphite effectively increased survival of Rhododendron species. It altered the composition of soil fungal communities, and the timing of using phosphite determined the way in which the fungal communities changed. Trichoderma taxa also responded to soil phosphite and Phytophthora cinnamomi. Conclusions The benefits of antagonistic fungi such as Trichoderma are context-dependent, suggesting protection against pathogens depends on the timing of phosphite application. This study provides evidence that phosphite-mediated pathogen protection includes both direct benefits to plants and indirect effects mediated through the soil fungal community.more » « less
- 
            The soil-borne pathogen Phytophthora cinnamomi causes a deadly plant disease. Phosphite is widely used as an effective treatment to protect plants from Phytophthora cinnamomi. Phosphite as a common fungicide might influence the composition of soil fungal communities. However, whether the belowground mechanisms of phosphite-mediated protections are direct or indirectly mediated through soil biota are unknown. Therefore, exploring belowground mechanisms could contribute to the evaluation of the sustainability of phosphite use and tests hypotheses about direct versus indirect mechanisms in pathogen response. Our greenhouse pot experiment on Rhododendron species had either an after-pathogen or a before-pathogen use of phosphite to compare and evaluate plant and soil fungal responses to phosphite and the presence of an oomycete pathogen phytophthora cinnamomi. The factorial experiment also included with and without pathogen and soil biota treatments, for a test of interactive effects. High throughput sequencing analyzed the soil fungal communities, and we measured the diversity, evenness and richness of soil fungi. Phosphite effectively increased survival of Rhododendron species. It altered the composition of soil fungal communities, and the timing of using phosphite determined the way in which the fungal communities changed. Trichoderma taxa also responded to soil phosphite and Phytophthora cinnamomi. The benefits of antagonistic fungi such as Trichoderma are context-dependent, suggesting protection against pathogens depends on the timing of phosphite application. This study provides the first evidence that phosphite-mediated pathogen protection includes both direct benefits to plants and indirect effects mediated through the soil microbial community.more » « less
 An official website of the United States government
An official website of the United States government 
				
			 
					 
					
 
                                    