The Context-Dependency of Plant-Microbial Interactions in the Bioenergy Resource Economy
Authors:
Rachel Hestrin1,2* (rhestrin@umass.edu), John Casey1, Rachel Hammer3, Noah Luecke3, Vanessa Brisson1, Megan Kan1, Rebecca Ju1, Jeffrey Kimbrel1, Christina Ramon1, Prasun Ray4, Rina Estera-Molina1,6, Jessica Wollard1, Marissa Lafler1, Steven Blazewicz1, Kelly Craven4,5, Mary Firestone6, Peter Weber1, Ali Navid1, Rhona Stuart1, Christine Hawkes3, Jennifer Pett-Ridge1, and Erin Nuccio1
Institutions:
1Lawrence Livermore National Laboratory; 2University of Massachusetts–Amherst; 3North Carolina State University (NCSU); 4Noble Research Institute; 5Oklahoma State University; and 6University of California–Berkeley
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 SFA seeks to understand phototroph-heterotroph interactions that shape productivity, robustness, the balance of resource fluxes, and the functionality of the surrounding microbiome. The team hypothesizes that different microbial associates not only have differential effects on host productivity but can change an entire system’s resource economy. The approach encompasses single cell analyses, quantitative isotope tracing of elemental exchanges, omics measurements, and multi-scale modeling to characterize microscale impacts on system-scale processes. The team aims to uncover crosscutting principles that regulate these interactions and their resource allocation consequences to develop a general predictive framework for system-level impacts of microbial partnerships.
Abstract
The hyphosphere is a hotspot for multipartite interactions that shape critical terrestrial processes such as soil nutrient cycling, C distribution, and plant growth. To investigate how water limitation impacts microbial dynamics and biogeochemistry in both the rhizosphere and hyphosphere, researchers inoculated P. hallii with one of two functionally different mycorrhizal partners (Rhizophagus irregularis and Serendipita bescii) and grew the plants under either water-limiting or water-replete conditions in 13CO2 labeling chambers to enable carbon tracking. After 3 months, researchers used H218O quantitative stable isotope probing (qSIP) to assess how water limitation impacted hyphosphere bacterial growth rates and diversity. The team found that both fungal partners helped sustain growth and diversity in hyphosphere bacterial communities exposed to water limitation relative to uninoculated controls. Of the bacterial taxa that responded positively to R. irregularis or S. bescii in water-limited soil, many belong to lineages that are considered drought-susceptible, including Bacteroidetes, Planctomycetes, Verrucomicrobia, Proteobacteria, and Acidobacteria. The size of soil C pools and 13CO2 efflux from hyphosphere soil depended on soil moisture conditions, but exometabolite profiles and multimodal imaging suggest that the different mycorrhizal fungi also can influence C flow and soil biogeochemistry. Together, the findings indicate that mycorrhizal fungi can support biotic activity and resilience to water limitation.
In addition to mycorrhizal fungi, roots are often colonized by a diverse array of endophytic fungi. Historically, these fungi have been assumed to be largely commensal, but recent work by the NCSU team suggests that many confer nutritional benefits to the host plant. Using a panel of phylogenetically diverse root endophytes isolated from switchgrass, researchers demonstrated that these fungi broadly enable plant acquisition of organic N and P in soil. Compared to fungus-free controls, 30% of fungi (n=12) increased tissue N by 20-90% when provided with organic N, and 40% of fungi (n=16) increased tissue P by 25-80%. Most importantly, some fungi appear to substantially shift the N:P ratio (from N>>P to N=P). Fungi that aggressively consumed organic nutrients in culture were less beneficial for host acquisition of organic N or P (r = -0.39 to -0.57). Leveraging these results, team members are investigating C-nutrient trading in the root endophyte system. This work will substantially increase understanding of root endophyte contributions to host and ecosystem C and nutrient cycling.
In parallel with experimental work, team members are developing a plant-mycorrhizal-bacteria model to bridge cellular scale processes within a systems-level context. The model is a hybrid model that combines a lattice-free hyphal network and a co-localized diffusive/advective grid. The model is designed to enable interpretation of and integration with spatially resolved community flux balance simulations of mycorrhizal-bacterial communities using data from experimental studies. Environmental control on plant, mycelium, and bacterial dynamics are governed by a set of coupled differential equations that preserve C and nutrient mass balances. The team will explore the traits and tradeoffs that promote plant growth and total system biomass growth under different environmental conditions and will test these predictions in future experimental studies.
Funding Information
This work was performed under the auspices of the U.S. Department of Energy at Lawrence Livermore National Laboratory under Contract DE-AC52- 07NA27344 and supported by the Genome Sciences Program of the Office of Biological and Environmental Research under the LLNL Biofuels SFA, FWP SCW1039, LLNL-ABS-845280.