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1. Home-field advantage affects the local adaptive interaction between Andropogon gerardii ecotypes and root-associated bacterial communities

   https://doi.org/10.1128/spectrum.00208-23  

   Kazarina, Anna; Sarkar, Soumyadev; Thapa, Shiva; Heeren, Leah; Kamke, Abgail; Ward, Kaitlyn; Hartung, Eli; Ran, Qinghong; Galliart, Matthew; Jumpponen, Ari; et al (October 2023, Microbiology Spectrum)

   Arias, Renee S. (Ed.)

   ABSTRACT Due to climate change, drought frequencies and severities are predicted to increase across the United States. Plant responses and adaptation to stresses depend on plant genetic and environmental factors. Understanding the effect of those factors on plant performance is required to predict species’ responses to environmental change. We used reciprocal gardens planted with distinct regional ecotypes of the perennial grassAndropogon gerardiiadapted to dry, mesic, and wet environments to characterize their rhizosphere communities using 16S rRNA metabarcode sequencing. Even though the local microbial pool was the main driver of these rhizosphere communities, the significant plant ecotypic effect highlighted active microbial recruitment in the rhizosphere, driven by ecotype or plant genetic background. Our data also suggest that ecotypes planted at their homesites were more successful in recruiting rhizosphere community members that were unique to the location. The link between the plants’ homesite and the specific local microbes supported the “home field advantage” hypothesis. The unique homesite microbes may represent microbial specialists that are linked to plant stress responses. Furthermore, our data support ecotypic variation in the recruitment of congeneric but distinct bacterial variants, highlighting the nuanced plant ecotype effects on rhizosphere microbiome recruitment. These results improve our understanding of the complex plant host–soil microbe interactions and should facilitate further studies focused on exploring the functional potential of recruited microbes. Our study has the potential to aid in predicting grassland ecosystem responses to climate change and impact restoration management practices to promote grassland sustainability. IMPORTANCEIn this study, we used reciprocal gardens located across a steep precipitation gradient to characterize rhizosphere communities of distinct dry, mesic, and wet regional ecotypes of the perennial grassAndropogon gerardii. We used 16S rRNA amplicon sequencing and focused oligotyping analysis and showed that even though location was the main driver of the microbial communities, ecotypes could potentially recruit distinct bacterial populations. We showed that differentA. gerardiiecotypes were more successful in overall community recruitment and recruitment of microbes unique to the “home” environment, when growing at their “home site.” We found evidence for “home-field advantage” interactions between the host and host–root-associated bacterial communities, and the capability of ecotypes to recruit specialized microbes that were potentially linked to plant stress responses. Our study aids in a better understanding of the factors that affect plant adaptation, improve management strategies, and predict grassland function under the changing climate. 

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2. Manipulating plant microbiomes in the field: Native mycorrhizae advance plant succession and improve native plant restoration

   https://doi.org/10.1111/1365-2664.14036  

   Koziol, Liz; Bauer, Jonathan T.; Duell, Eric B.; Hickman, Karen; House, Geoffrey L.; Schultz, Peggy A.; Tipton, Alice G.; Wilson, Gail W. T.; Bever, James D. (October 2021, Journal of Applied Ecology)

   Abstract The plant microbiome is critical to plant health and is degraded with anthropogenic disturbance. However, the value of re‐establishing the native microbiome is rarely considered in ecological restoration. Arbuscular mycorrhizal (AM) fungi are particularly important microbiome components, as they associate with most plants, and later successional grassland plants are strongly responsive to native AM fungi.With five separate sites across the United States, we inoculated mid‐ and late successional plant seedlings with one of three types of native microbiome amendments: (a) whole rhizosphere soil collected from local old‐growth, undisturbed grassland communities in Illinois, Kansas or Oklahoma, (b) laboratory cultured AM fungi from these same old‐growth grassland sites or (c) no microbiome amendment. We also seeded each restoration with a diverse native seed mixture. Plant establishment and growth was followed for three growing seasons.The reintroduction of soil microbiome from native ecosystems improved restoration establishment.Including only native arbuscular mycorrhizal fungal communities produced similar improvements in plant establishment as what was found with whole soil microbiome amendment. These findings were robust across plant functional groups.Inoculated plants (amended with either AM fungi or whole soil) also grew more leaves and were generally taller during the three growing seasons.Synthesis and applications. Our research shows that mycorrhizal fungi can accelerate plant succession and that the reintroduction of both whole soil and laboratory cultivated native mycorrhizal fungi can be used as tools to improve native plant restoration following anthropogenic disturbance. 

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3. Native Microbes Amplify Native Seedling Establishment and Diversity While Inhibiting a Non-Native Grass

   https://doi.org/10.3390/plants12051184  

   Koziol, Liz; McKenna, Thomas P.; Bever, James D. (March 2023, Plants)

   Although several studies have shown increased native plant establishment with native microbe soil amendments, few studies have investigated how microbes can alter seedling recruitment and establishment in the presence of a non-native competitor. In this study, the effect of microbial communities on seedling biomass and diversity was assessed by seeding pots with both native prairie seeds and a non-native grass that commonly invades US grassland restorations, Setaria faberi. Soil in the pots was inoculated with whole soil collections from ex-arable land, late successional arbuscular mycorrhizal (AM) fungi isolated from a nearby tallgrass prairie, with both prairie AM fungi and ex-arable whole soil, or with a sterile soil (control). We hypothesized (1) late successional plants would benefit from native AM fungi, (2) that non-native plants would outcompete native plants in ex-arable soils, and (3) early successional plants would be unresponsive to microbes. Overall, native plant abundance, late successional plant abundance, and total diversity were greatest in the native AM fungi+ ex-arable soil treatment. These increases led to decreased abundance of the non-native grass S. faberi. These results highlight the importance of late successional native microbes on native seed establishment and demonstrate that microbes can be harnessed to improve both plant community diversity and resistance to invasion during the nascent stages of restoration. 

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4. Ectomycorrhizal fungi alter soil food webs and the functional potential of bacterial communities

   https://doi.org/10.1128/msystems.00369-24  

   Berrios, Louis; Bogar, Glade D; Bogar, Laura M; Venturini, Andressa M; Willing, Claire E; Del_Rio, Anastacia; Ansell, T Bertie; Zemaitis, Kevin; Velickovic, Marija; Velickovic, Dusan; et al (May 2024, mSystems)

   Gao, Cheng (Ed.)

   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. 

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5. Inoculation with native soil improves seedling survival and reduces non‐native reinvasion in a grassland restoration

   https://doi.org/10.1111/rec.13685  

   Duell, Eric B.; O'Hare, Anna; Wilson, Gail W. T. (April 2022, Restoration Ecology)

   Losses of grasslands have been largely attributed to widespread land‐use changes, such as conversion to row‐crop agriculture. The remaining tallgrass prairie faces further losses due to biological invasions by non‐native plant species, often with resultant ecosystem degradation. Of critical concern for conservation, restoration of native grasslands has been met with little success following eradication of non‐native plants. In addition to the direct and indirect effects of non‐native invasive plants on beneficial soil microbes, management practices targeting invasive species may also negatively affect subsequent restoration efforts. To assess mechanisms limiting germination and survival of native species and to improve native species establishment, we established six replicate plots of each of the following four treatments: (1) inoculated with freshly collected prairie soil with native seeds; (2) inoculated with steam‐pasteurized soil with native seeds; (3) noninoculated with native seeds; or (4) noninoculated/nonseeded control. Inoculation with whole soil did not improve seed germination; however, addition of whole soil significantly improved native species survival, compared to pasteurized soil or noninoculated treatments. Inoculation with whole soil significantly decreased reestablishment of non‐native invasiveBothriochloa bladhii(Caucasian bluestem); at the end of the growing season, plots receiving whole soil consisted of approximately 30%B. bladhiicover, compared to approximately 80% in plots receiving no soil inoculum. Our results suggest invasion and eradication efforts negatively affect arbuscular mycorrhizal hyphal and spore abundances and soil aggregate stability, and inoculation with locally adapted soil microbial communities can improve metrics of restoration success, including plant species richness and diversity, while decreasing reinvasion by non‐native species. 

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