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Agriculture is driving biodiversity loss, and future bioenergy cropping systems have the potential to ameliorate or exacerbate these effects. Using a long-term experimental array of 10 bioenergy cropping systems, we quantified diversity of plants, invertebrates, vertebrates, and microbes in each crop. For many taxonomic groups, alternative annual cropping systems provided no biodiversity benefits when compared to corn (the business-as-usual bioenergy crop in the United States), and simple perennial grass–based systems provided only modest gains. In contrast, for most animal groups, richness in plant-diverse perennial systems was much higher than in annual crops or simple perennial systems. Microbial richness patterns were more eclectic, although some groups responded positively to plant diversity. Future agricultural landscapes incorporating plant-diverse perennial bioenergy cropping systems could be of high conservation value. However, increased use of annual crops will continue to have negative effects, and simple perennial grass systems may provide little improvement over annual crops.

 

As microbiome research has progressed, it has become clear that most, if not all, eukaryotic organisms are hosts to microbiomes composed of prokaryotes, other eukaryotes, and viruses. Fungi have only recently been considered holobionts with their own microbiomes, as filamentous fungi have been found to harbor bacteria (including cyanobacteria), mycoviruses, other fungi, and whole algal cells within their hyphae. Constituents of this complex endohyphal microbiome have been interrogated using multi-omic approaches. However, a lack of tools, techniques, and standardization for integrative multi-omics for small-scale microbiomes (e.g., intracellular microbiomes) has limited progress towards investigating and understanding the total diversity of the endohyphal microbiome and its functional impacts on fungal hosts. Understanding microbiome impacts on fungal hosts will advance explorations of how “microbiomes within microbiomes” affect broader microbial community dynamics and ecological functions. Progress to date as well as ongoing challenges of performing integrative multi-omics on the endohyphal microbiome is discussed herein. Addressing the challenges associated with the sample extraction, sample preparation, multi-omic data generation, and multi-omic data analysis and integration will help advance current knowledge of the endohyphal microbiome and provide a road map for shrinking microbiome investigations to smaller scales.

 

Members of the fungal genusMorchellaare widely known for their important ecological roles and significant economic value. In this study, we used amplicon and genome sequencing to characterize bacterial communities associated with sexual fruiting bodies from wild specimens, as well as vegetative mycelium and sclerotia obtained fromMorchellaisolates grownin vitro. These investigations included diverse representatives from both Elata and EsculentaMorchellaclades. Unique bacterial community compositions were observed across the various structures examined, both within and across individualMorchellaisolates or specimens. However, specific bacterial taxa were frequently detected in association with certain structures, providing support for an associated core bacterial community. Bacteria from the genusPseudomonasandRalstoniaconstituted the core bacterial associates ofMorchellamycelia and sclerotia, while other genera (e.g.,Pedobacterspp.,Deviosaspp., andBradyrhizobiumspp.) constituted the core bacterial community of fruiting bodies. Furthermore, the importance ofPseudomonasas a key member of the bacteriome was supported by the isolation of severalPseudomonasstrains from mycelia duringin vitrocultivation. Four of the six mycelial-derivedPseudomonasisolates shared 16S rDNA sequence identity with amplicon sequences recovered directly from the examined fungal structures. Distinct interaction phenotypes (antagonistic or neutral) were observed in confrontation assays between these bacteria and variousMorchellaisolates. Genome sequences obtained from thesePseudomonasisolates revealed intriguing differences in gene content and annotated functions, specifically with respect to toxin-antitoxin systems, cell adhesion, chitinases, and insecticidal toxins. These genetic differences correlated with the interaction phenotypes. This study provides evidence thatPseudomonasspp. are frequently associated withMorchellaand these associations may greatly impact fungal physiology.

 

Terpenes are among the oldest and largest class of plant-specialized bioproducts that are known to affect plant development, adaptation, and biological interactions. While their biosynthesis, evolution, and function in aboveground interactions with insects and individual microbial species are well studied, how different terpenes impact plant microbiomes belowground is much less understood. Here we designed an experiment to assess how belowground exogenous applications of monoterpenes (1,8-cineole and linalool) and a sesquiterpene (nerolidol) delivered through an artificial root system impacted its belowground bacterial and fungal microbiome. We found that the terpene applications had significant and variable impacts on bacterial and fungal communities, depending on terpene class and concentration; however, these impacts were localized to the artificial root system and the fungal rhizosphere. We complemented this experiment with pure culture bioassays on responsive bacteria and fungi isolated from the sorghum rhizobiome. Overall, higher concentrations (200 µM) of nerolidol were inhibitory toFerrovibriumand tested Firmicutes. While fungal isolates ofPenicilliumandPericoniawere also more inhibited by higher concentrations (200 µM) of nerolidol,Clonostachyswas enhanced at this higher level and together withHumicolawas inhibited by the lower concentration tested (100 µM). On the other hand, 1,8-cineole had an inhibitory effect onOrbiliaat both tested concentrations but had a promotive effect at 100 µM onPenicilliumandPericonia. Similarly, linalool at 100 µM had significant growth promotion inMortierella, but an inhibitory effect forOrbilia. Together, these results highlight the variable direct effects of terpenes on single microbial isolates and demonstrate the complexity of microbe-terpene interactions in the rhizobiome.

Terpenes represent one of the largest and oldest classes of plant-specialized metabolism, but their role in the belowground microbiome is poorly understood. Here, we used a “rhizobox” mesocosm experimental set-up to supply different concentrations and classes of terpenes into the soil compartment with growing sorghum for 1 month to assess how these terpenes affect sorghum bacterial and fungal rhizobiome communities. Changes in bacterial and fungal communities between treatments belowground were characterized, followed by bioassays screening on bacterial and fungal isolates from the sorghum rhizosphere against terpenes to validate direct microbial responses. We found that microbial growth stimulatory and inhibitory effects were localized, terpene specific, dose dependent, and transient in time. This work paves the way for engineering terpene metabolisms in plant microbiomes for improved sustainable agriculture and bioenergy crop production.