Genomic Science Program
U.S. Department of Energy | Office of Science | Biological and Environmental Research Program

Beneficial Plant-Fungal Partnerships in the Resource Economy of Bioenergy Grasses

Authors:

Erin Nuccio2* (nuccio1@llnl.gov); John Casey2*(casey26@llnl.gov); Rachel Hestrin1,2, Jeffrey Kimbrel2, Megan Kan2, Vanessa Brisson2, Rebecca Ju2, Joshua White2, Corentin Bisot3, Christina Ramon2, Jessica Wollard2, Marissa Lafler2, Prasun Ray4,5, Katerina Estera-Molina2,6, Steven Blazewicz1, Kelly Craven5,6, Mary Firestone6, Ali Navid2, Rhona Stuart2, Peter Weber2, E. Toby Kiers7, Jennifer Pett-Ridge2,8

Institutions:

1University of Massachusetts–Amherst; 2Lawrence Livermore National Laboratory; 3AMOLF Institute Netherland–Netherlands; 4University of Maryland Eastern Shore–Princess Anne; 5Noble Research Institute–Ardmore; 6University of California–Berkeley; 6Oklahoma State University–Stillwater; 7Vrije Universiteit Amsterdam–Netherlands; 8University of California Merced, Life and Environmental Sciences Department–Merced

URLs:

Goals

Algal and plant systems have the unrivaled advantage of converting solar energy and CO2 into useful organic molecules. Their growth and efficiency are largely shaped by the microbial communities in and around them. The μBiospheres Science Focus Area seeks to understand phototroph-heterotroph interactions that shape productivity, robustness, the balance of resource fluxes, and the functionality of the surrounding microbiome. Researchers hypothesize that different microbial associates not only have differential effects on host productivity but can change an entire system’s resource economy. This approach encompasses single-cell analyses, quantitative isotope tracing of elemental exchanges, omics measurements, and multiscale modeling to characterize microscale impacts on system-scale processes. Researchers aim to uncover cross-cutting principles that regulate these interactions and their resource allocation consequences to develop a general predictive framework for system-level impacts of microbial partnerships.

Abstract

Multipartite mutualisms between plants and microbiota can enhance plant productivity, stress resilience, and carbon (C) allocation belowground. Researchers are investigating context-dependent mutualisms between Panicum virgatum (switchgrass, a cellulosic bioenergy grass), Panicum hallii (a model for bioenergy grasses), and mycorrhizal and endophytic fungi. The team is interested in how C flows are mediated by plant-associated fungi and altered by environmental stress (e.g., drought). In return, it is thought that hyphosphere microbes surrounding fungal hyphae enable root-associated fungi to obtain resources (N, P, H2O) that they provide to their hosts, but the mechanisms that enable this crosskingdom cooperation are unknown. Researchers are investigating these questions using (1) 13CO2 stable isotope probing (SIP) and metabolomics; and (2) live imaging and spatial metabolomics coupled to metabolic modeling.

Fungal root endophytes can alleviate plant drought stress, but their effects on soil microbial activity and C flows during drought are poorly understood. The team used 13CO2 labeling chambers, root exclusion cores, quantitative SIP (qSIP), and metabolomics to investigate how two functionally distinct root endophytes influenced rhizosphere and hyphosphere C dynamics in moisture-limited soils planted with P. hallii. Researchers compared the arbuscular mycorrhizal fungus (AMF) Rhizophagus irregularis, with a Sebacinales endophytic fungus Serendipita bescii. CO2 efflux and 13CO2 efflux were greater from fungal inoculated versus uninoculated soils, indicating that these fungi facilitated faster turnover of both native soil organic matter and 13C photosynthates. However, the team did not measure a net reduction in total soil C. Microbial 13C assimilation was greater in fungal-inoculated soil, and a distinct microbial consortia assimilated 13C in each treatment. The hyphosphere exometabolome was primarily structured by time and was distinct between well-watered and drought conditions; a subset of metabolites differed by the specific fungal partner inoculation. These results provide a putative mechanism to explain the previous observation that fungal-root endophytes help maintain bacterial growth potential, growth efficiency, and diversity following moisture limitation (Hestrin et al. 2022).

Fungal exudates are a key form of C in the hyphosphere and may mediate a metabolomic conversation between fungi and their microbiome. To relate fungal network development and exudation to microbiome nutrient acquisition, researchers are coupling spatially resolved analyses to a metabolic modeling simulation platform called “Toadstool.” These experiments start with automated live imaging and network identification to generate baseline structural data for Toadstool. Toadstool is built on a stochastic network representation of R. irregularis growth and resource allocation in soil, coupled to differential equations that represent light- and nutrient-dependent growth of P. virgatum. Currently, researchers are developing a method to spatially map AMF metabolites using matrix-assisted laser desorption and ionization (MALDI) that can pair with live-imaging data. Toadstool was designed to interact within a diffusive and advective grid, allowing a direct interface with spatially resolved metabolic models of R. irregularis hyphae and their bacterial partners. This approach enables a comparison of predicted metabolite exchanges with MALDI metabolite imaging. The model is intended to predict feedbacks between growth, plant-AMF-bacterial community resource exchange, and the soil matrix. This work will shed light on how multipartite biological interactions impact the soil resource economy.

References

Hestrin, R., et al. 2022. “Plant-Associated Fungi Support Bacterial Resilience Following Water Limitation,” The ISME Journal 1–11.

Funding Information

This work was performed under the auspices of the DOE at Lawrence Livermore National Laboratory (LLNL) under contract DE-AC52- 07NA27344 and supported by the Genome Sciences Program of the BER program under the LLNL Biofuels Science Focus Area, FWP SCW1039.