Microbial community dynamics responding to nutrient allocation associated with soybean cultivar ‘Jake’ ozone adaptation

Authors: ZHANG, KAILE - University Of Florida; Zentella, Rodolfo; Burkey, Kent; LIAO, HUI-LING - University Of Florida; Tisdale, Ripley

Submitted to: Science of the Total Environment
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 12/13/2022
Publication Date: 12/19/2022
Citation: Zhang, K., Zentella Gomez, R., Burkey, K.O., Liao, H., Tisdale, R.H. 2022. Microbial community dynamics responding to nutrient allocation associated with soybean cultivar ‘Jake’ ozone adaptation. Science of the Total Environment. 864:161008. https://doi.org/10.1016/j.scitotenv.2022.161008.
DOI: https://doi.org/10.1016/j.scitotenv.2022.161008

Interpretive Summary: Ozone pollution is a major environmental threat to global ecosystems and food security. Soybean is a major US staple crop, with exports valued at $18.7 billion. However, soybean production has come under growing ozone threat and now faces a steep reduction in annual yield of more than 15%. To confront this environmental challenge, optimize crop yields, and maintain food sources for a growing US and global population, breeders and plant researchers are working to develop crops that can withstand environmental stresses and support healthy ecosystems. To this end, USDA-ARS PSRU scientists in Raleigh, North Carolina have recently identified ‘Jake’ as a highly productive, ozone-resilient soybean cultivar. In this research, we took further steps to understand how soil microbes assist ‘Jake’ in adapting to elevated ozone environments. This study demonstrated that ozone did not alter soil bacteria composition throughout ‘Jake’ development but significantly decreased the diversity of symbiotic fungi. By investigating the correlation between microbial networks and nutrient allocation, this study identified some symbiotic bacteria and fungi that may support soybean ozone adaptation. This research will provide knowledge regarding soil microorganisms under elevated ozone and identify potential soil microbes that can enhance the performance of crops under environmental stresses and thereby substantially improve agroecosystems.

Technical Abstract: Tropospheric ozone (O3), a major air pollutant, leads to significant global yield loss in soybean [Glycine max (L.) Merr.]. Soybean cultivar ‘Jake’ shows O3 resilient traits in above-ground organs, but the root system remains sensitive to elevated O3 (eO3). Changing carbon (C) and nitrogen (N) resource composition during eO3 stress suggests that eO3 presumably alters belowground soil microbial communities and their driven nutrient transformation. Yet, the responses of belowground microbes to eO3 and their feedback on nutrient cycling in ‘Jake’ are unknown. In this study, we holistically investigated soil microbial communities associated with C and N dynamics and bacterial-fungal inter-kingdom networks in the rhizosphere and bulk soil at different developmental stages of ‘Jake’ grown under sub-ambient O3 [charcoal-filtered (CF) air, 12 h mean: 20 ppb] or eO3 (12 h mean: 87 ppb). The results demonstrated eO3 significantly decreased fungal diversity and complexity of microbial networks at different ‘Jake’ developmental stages, whereas bacterial diversity was more tolerant to eO3 in both bulk soil and rhizosphere. In the bulk soil, no O3-responsive microbial biomarkers were found to be associated with C and N content, implying eO3 may stimulate niche-based processes during ‘Jake’ growth. In contrast, this study identified O3-responsive microbial biomarkers that may contribute to the N acquisition (Chloroflexales) and C dynamics (Caldilineales, Thermomicrobiales, and Hypocreales) in the rhizosphere, which may support the O3 resilience of the ‘Jake’ cultivar. However, further investigation is required to confirm their specific contributions by determining changes in microbial gene expression. Overall, these findings conduce to an expanding knowledge base that O3 induces temporal and spatial changes in the effects of microbial and nutrient networks in the O3-tolerant agriculture ecosystems.