Drought shifts sorghum root metabolite and microbiome profiles and enriches for pipecolic acid

Authors: CADDELL, DANIEL - Non ARS Employee; PETTINGA, DEAN - University Of California Berkeley; LOUIE, KATHERINE - Lawrence Berkeley National Laboratory; BOWEN, BENJAMIN - Department Of Energy Joint Genome; SIEVERT, JULIE - Kearney Agricultural Center; HOLLINGSWORTH, JOY - Kearney Agricultural Center; RUBANOWITZ, REBECKAH - University Of California Berkeley; DAHLBERG, JEFFERY - Kearney Agricultural Center; PURDOM, ELIZABETH - University Of California Berkeley; NORTHEN, T - Lawrence Berkeley National Laboratory; Coleman-Derr, Devin

Submitted to: Phytobiomes Journal
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 8/22/2023
Publication Date: 12/13/2023
Citation: Caddell, D.F., Pettinga, D., Louie, K., Bowen, B.P., Sievert, J.A., Hollingsworth, J., Rubanowitz, R., Dahlberg, J., Purdom, E., Northen, T., Coleman-Derr, D.A. 2023. Drought shifts sorghum root metabolite and microbiome profiles and enriches for pipecolic acid. Phytobiomes Journal. 7(4):449-463. https://doi.org/10.1094/PBIOMES-02-23-0011-R.
DOI: https://doi.org/10.1094/PBIOMES-02-23-0011-R

Interpretive Summary: The soil microbiome carries out several important ecological functions including carbon cycling and plant growth promotion. Over the last several years the application of exogenous microbes to soil has expanded and has led to increases in agricultural output. However, the addition of new species to existing soil microbiomes opens up questions related to how added species can be contained to their intended roles and not persist outside their functional or geographic niches. Genomic reduction to remove key pathways, thereby hampering an organism’s ability to persist outside of a defined environment, is one avenue to promote containment. However, the possibility exists that the native soil microbiome may be able to complement these missing pathways either metabolically or genetically through horizontal gene transfer.

Technical Abstract: To begin to explore this possibility we have developed several synthetic communities that were derived from the native soil microbiome surrounding the rhizosphere of sorghum, a key bioenergy crop. These Synthetic Sorghum Communities (SSCs) were developed using a top-down approach and represent simplified, defined sets of microbial species that can act as a palette for genetic or metabolic complementation of added species. We show that SSCs are initially dynamic in their development before stabilizing and falling in complexity and richness. SSCs also represent powerful tools for the scientific community due to their ability to be stored and reproducibly reconstituted as we show here. Individual isolates from SSCs show a range of growth profiles across several carbon sources, highlighting the potential of SSCs to serve as complementation palettes. Finally, we show that some SSCs are amenable to incorporation by new species that they were not evolved with, but this incorporation is variable. These experiments reveal how SSCs can be generated and stored and begin to show the species and carbon utilization pathways that represent the most common routes of potential metabolic complementation. We also show that incorporation of new species is not a guarantee suggesting that complementation may be the exception, rather than the rule. Future experiments will focus on incubation of genomically reduced species with SSCs to explore their complementation effects, pathways and kinetics, improving our ability to control persistence of modified bacterial species in native soil systems.