Shifts in soil bacterial communities as a function of carbon source used during anaerobic soil disinfestation

Authors: Poret-Peterson, Amisha; ALBU, SEBASTIAN - California Department Of Food And Agriculture; McClean, Ali; Kluepfel, Daniel

Submitted to: Frontiers in Environmental Science
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 12/18/2018
Publication Date: 1/9/2019
Citation: Poret-Peterson, A.T., Albu, S., McClean, A.E., Kluepfel, D.A. 2019. Shifts in soil bacterial communities as a function of carbon source used during anaerobic soil disinfestation. Frontiers in Environmental Science. 6:160. https://doi.org/10.3389/FENVS.2018.00160.
DOI: https://doi.org/10.3389/FENVS.2018.00160

Interpretive Summary: The use of pre-plant chemical fumigation of soil to manage soil-borne plant pathogens in a variety of cropping systems is increasingly restricted due to environmental impacts and human health concerns. Hence, alternatives to chemical fumigation are needed. Anaerobic soil disinfestation (ASD) is an alternative management tool that is gaining considerable interest for tree crop production. ASD involves generating anaerobic conditions in soil through amendment with an organic carbon source, irrigation to field capacity, and covering soil with a gas impermeable plastic tarp. Pathogen suppression appears to be carbon-source dependent and mediated by bacteria that produce volatile organic compounds and physical and chemical changes in the soil, such as elevated temperature, lowered pH and redox potential, etc. The standard carbon source for ASD is rice bran. The carbon source used is one key determinant of the effectiveness of ASD and offers an opportunity to tailor ASD for particular crops, soil types, localities, or target plant pathogens. In this study, we conducted replicated field trials of ASD using rice bran and other agricultural by-products to (1) determine if we would observe similar bacterial community shifts between the carbon sources and (2) assess if the bacterial community shifts would be consistent between trials. We found that rice bran and the other agricultural by-products tested significantly increased the abundances of a core group of anaerobic bacterial taxa (i.e., Clostridiales and Selenomonadeles) in both trials. These bacterial taxa have the genomic potential to produce compounds previously shown to inhibit growth of plant pathogens. These results indicate that reproducible and effective implementation of ASD is achievable with alternative carbon substrates to rice bran.

Technical Abstract: Anaerobic soil disinfestation (ASD) is an organic amendment-based management practice for controlling soil-borne plant pathogens. Pathogen suppression appears to be carbon source-dependent and mediated by bacteria that proliferate and produce volatile organic compounds, as well as physico-chemical changes (i.e., elevated temperature, lowered redox potential and pH, release of metal ions) in soil. ASD is under study for adoption in tree crops as a replacement for chemical-fumigation, but its widespread use is limited by incomplete understanding of its suppression mechanisms and high economic costs. The carbon substrate used to induce ASD is one component of the process that can be optimized to enhance effectiveness and affordability. Rice bran is the standard carbon source for ASD and we identified three other substrates (molasses, mustard seed meal, and tomato pomace) that are similar in efficacy to rice bran at generating and sustaining soil anoxia and reducing the population of an introduced plant pathogen. Here, we used replicated field trials of ASD to determine if rice bran and the alternative carbon substrates would elicit similar soil bacterial communities (characterized via amplicon sequencing of the 16S rRNA gene v4 region) and to assess if any observed community shifts were consistent across the repeated trials. We found significant but minimal differences in community composition between ASD carbon treatments (F4,30 = 2.80, P < 0.001, R2 = 0.22) and trials (F1,30 = 5.24, P < 0.001, R2 = 0.10). In both trials, the abundances of Bacteroidales, Clostridiales, Selenomonadales, and Enterobacteriales increased significantly (> 5 log2 fold change) in all ASD treatments compared to untreated controls. A group of shared core genera belonging to the Clostridiales and Selenomonadales were identified in both trials and constituted 22.6% and 21.5% of the communities. Bacterial taxa that were most responsive to ASD treatments had the genomic potential for fermentation reactions that produce organic acids (such as acetate and butyrate) known to inhibit the in vitro growth of plant pathogens, denitrification, and nitrogen fixation based on predicted metagenomes. Taken together, these results indicate that reproducible and effective implementation of ASD is achievable with alternative carbon substrates to rice bran.