Manipulating atmospheric CO2 concentration induces shifts in wheat leaf and spike microbiomes and in Fusarium pathogen communities

Authors: BAKKER, MATTHEW - University Of Manitoba; Whitaker, Briana; McCormick, Susan; Ainsworth, Elizabeth - Lisa; Vaughan, Martha

Submitted to: Frontiers in Microbiology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 9/25/2023
Publication Date: 10/10/2023
Citation: Bakker, M.G., Whitaker, B.K., McCormick, S.P., Ainsworth, E.A., Vaughan, M.M. 2023. Manipulating atmospheric CO2 concentration induces shifts in wheat leaf and spike microbiomes and in Fusarium pathogen communities. Frontiers in Microbiology. 14. Article 1271219. https://doi.org/10.3389/fmicb.2023.1271219.
DOI: https://doi.org/10.3389/fmicb.2023.1271219

Interpretive Summary: The microbial communities living on crops can greatly contribute to overall plant health and productivity, but it remains unclear how rising atmospheric CO2 will affect the crop microbiome – including its pathogens such as Fusarium. Fusarium fungi can cause Fusarium Head Blight (FHB) of wheat and other cereal crops. FHB results in billions of dollars in annual yield losses and results in grain contamination with a toxin that makes it unsafe to eat. ARS researchers in Peoria, Illinois, in collaboration with a scientist at the University of Manitoba, evaluated the effect of rising CO2 on microbial communities of wheat grown in a free air CO2 enrichment field and discovered that elevated CO2 changes the bacterial and fungal microbiome. However, the changes varied within and between years. Interestingly, the abundance of Fusarium was also altered by atmospheric CO2, but the effect was strain specific with one strain of Fusarium showing increased abundance under elevated relative to ambient atmospheric CO2, while a second strain of Fusarium was reduced in abundance at elevated atmospheric CO2. This knowledge can be applied to help understand how microbes are likely to respond to rising atmospheric CO2 and indicate that certain Fusarium strains will gain an advantage and become more abundant.

Technical Abstract: The changing composition of the atmosphere represents a source of uncertainty in our understanding of plant-microbe interactions, including assessment of future disease risks particularly in the context of mycotoxin producing fungal pathogens which are predicted to be more problematic with climate change. To address this uncertainty, we profiled microbiomes and compared the dynamics of naturally infecting versus artificially introduced Fusarium spp. on wheat plants grown under ambient vs. elevated atmospheric carbon dioxide concentration [CO2] in a field setting over two years. We found that the well-known temporal dynamics of plant-associated microbiomes were affected by [CO2]. The abundances of many amplicon sequence variants (a proxy for different microbial strains) significantly differed in elevated [CO2], often in an interactive manner with date of sample collection or with tissue type. In addition, we found evidence that two strains of Fusarium – an important group of mycotoxin producing plant fungal pathogens – responded to changes in [CO2]. The two sequence variants mapped to different phylogenetic subgroups within the genus Fusarium and had differential [CO2] responses. This work informs our understanding of how plant-associated microbiomes and pathogens may respond to on-going global change.