Temporal dynamics of the soil metabolome and microbiome during simulated anaerobic soil disinfestation

Authors: HEWAVITHARANA, SHASHIKA - Washington State University; KLARER, EMMI - Washington State University; Reed, Andrew; Leisso, Rachel; Poirier, Brenton; Honaas, Loren; Rudell, David; Mazzola, Mark

Submitted to: Frontiers in Microbiology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 9/30/2019
Publication Date: 10/15/2019
Citation: Hewavitharana, S., Klarer, E., Reed, A.J., Leisso, R.S., Poirier, B.C., Honaas, L.A., Rudell Jr, D.R., Mazzola, M. 2019. Temporal dynamics of the soil metabolome and microbiome during simulated anaerobic soil disinfestation. Frontiers in Microbiology. 10. https://doi.org/10.3389/fmicb.2019.02365.
DOI: https://doi.org/10.3389/fmicb.2019.02365

Interpretive Summary: Understanding the means by which the process of anaerobic soil disinfestation provides soil-borne disease control is an important step to garnering the ability to use the non-fumigant strategy in commercial crop production systems. In this study we demonstrated that carbon source is a key factor that drives changes in soil chemistry, microbiome composition and metabolic transformations during the ASD treatment. Time-series analysis of the microbiome and metabolome allowed for detection of both gradual and punctuated changes in the soil system while highlighting associations between specific microbial groups and the production of specific metabolites in the soil that potentially contribute to disease suppression. While previous studies have focused on both biological and chemical modes of disease suppression, limitations such as measuring this elements only at a single terminal sampling time point, sole focus on organic acids, or changes only in bacterial populations, with exclusion of fungal populations, hindered overall understanding of functional attributes of ASD. In the current study, these aspects were addressed, and potential new modes of action (i.e. fungistatic features of hydrocarbons and p-cresol) were suggested. Findings in this study provide more direction for field application of ASD. For instance, significance of labile carbon source to increase the rate of attainment of anaerobicity and minimum incubation period duration for generation of certain chemical modes of actions, such as methyl sulfides, have been unraveled in this study.

Technical Abstract: Significant interest exists in engineering the soil microbiome to attain suppression of soil-borne plant diseases. Anaerobic soil disinfestation (ASD) has potential as a biologically-regulated disease control method; however, the role of specific metabolites and microbial community dynamics contributing to ASD mediated disease control is mostly uncharacterized. Understanding the trajectory of co-evolutionary processes leading to syntrophic generation of functional metabolites during ASD is a necessary prelude to the predictive utilization of this management approach. Consequently, metabolic and microbial community profiling were used to generate highly dimensional datasets and network analysis to identify sequential transformations through aerobic, facultatively anaerobic, and anaerobic soil phases and distinct groups of metabolites and microorganisms linked with those. Proliferation and dynamic compositional changes in the Firmicutes community continued throughout the anaerobic phase and was linked to temporal changes in metabolite abundance including accumulation of small chain organic acids, methyl sulfide compounds, hydrocarbons, and p-cresol with antimicrobial properties. Novel potential modes of disease control during ASD were identified and the importance of the amendment and “community metabolism” for temporally supplying specific classes of labile compounds were revealed. To our knowledge this is the first study to report a comprehensive analysis of the soil metabolome, including classification of the polar, non-polar, and volatile metabolites generated during the course of ASD alongside changes in the soil microbiome.