Anaerobic soil disinfestation rather than Bacillus velezensis Y6 inoculant suppresses tomato bacterial wilt by improving soil quality and manipulating bacterial communities

doi:10.1016/j.jia.2024.06.019

Journal of Integrative Agriculture

2025, Vol. 24

Issue (2): 754-768 DOI: 10.1016/j.jia.2024.06.019

Agro-ecosystem & Environment

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Anaerobic soil disinfestation rather than Bacillus velezensis Y6 inoculant suppresses tomato bacterial wilt by improving soil quality and manipulating bacterial communities

Taowen Pan^{1, 2, 3}, Yulin Chen^{1, 2, 3}, Sicong Li^{1, 2, 3}, Lei Wang^{1, 2, 3}, Joji Muramoto⁴, Carol Shennan⁴, Jihui Tian^{1, 2, 3}, Kunzheng Cai^{1, 2, 3#}

¹Guangdong Provincial Key Laboratory of Eco-Circular Agriculture, South China Agricultural University, Guangzhou 510642, China

²Key Laboratory of Tropical Agricultural Environment in South China, Ministry of Agriculture and Rural Affairs, Guangzhou 510642, China

³College of Natural Resources and Environment, South China Agricultural University, Guangzhou 510642, China

⁴Environmental Studies, University of California Santa Cruz, Santa Cruz, CA 95064, United States

Highlights
● Anaerobic soil disinfestation (ASD) is an effective strategy to inhibit the occurrence of bacterial wilt.
● ASD improves soil quality and promotes the colonization of beneficial flora.
● ASD contributes to the improvement of bacterial community stability.
● The changes in soil bacterial community are mainly affected by ASD treatment.
● Soil pH is positively correlated with pathogens suppression.

Abstract
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摘要

连作导致了土传病害的发生，例如由青枯菌引起的青枯病，这给农业发展带来了风险。土壤厌氧消毒（ASD）和植物根际促生菌（PGPR）的施用被认为是控制青枯病的环境友好型方法。然而，ASD处理和PGPR接种后对改善土壤健康和抑制青枯病的潜在机制仍需要进一步探索。本研究评价了ASD处理对番茄种植前土壤改良的效果，以及ASD处理联合施用贝莱斯芽孢杆菌Y6（BV）对番茄收获前90天的土壤质量、青枯菌丰度和细菌群落的影响。结果表明，ASD处理使土壤中青枯菌的丰度在种植前降低17.6%，在收获前90天降低18.7%，但BV处理对此没有影响。在收获前90天，ASD和ASD+BV处理均有效降低青枯病的发生，改善土壤养分状况，并提高土壤微生物活性。主坐标分析表明，ASD处理显著影响土壤细菌群落结构在种植前和收获前90天。进一步研究发现，ASD处理有助于有益菌群（芽孢杆菌和链霉菌）的富集。此外，pH是影响土壤中青枯菌丰度的重要环境因子。有趣的是，共发生网络分析表明，ASD处理显著增加正相关关联和有益微生物（变形菌门和厚壁菌门）的比例，提高种植前和收获前90天的土壤细菌共发生网络复杂性。总之，这些结果表明，ASD处理而非微生物接种可以通过改善土壤质量和调控土壤细菌群落来增强番茄植株对青枯病的抗性。

Abstract

Continuous cropping leads to high incidence of soilborne diseases such as bacterial wilt caused by Ralstonia solanacearum, which poses a risk to agricultural production. Anaerobic soil disinfestation (ASD) and plant growth-promoting rhizobacteria (PGPR) are considered environmentally friendly methods to control bacterial wilt. However, the underlying mechanism of the improvement of soil health and the inhibition of bacterial wilt after ASD treatment and PGPR inoculation needs further exploration. This study evaluated the effect of ASD treatment on soil improvement at pre-planting of tomato, and the effect of ASD treatment combined with the application of Bacillus velezensis Y6 (BV) on soil quality, R. solanacearum abundance, and bacterial communities at 90 days before harvesting of tomato. The results showed that ASD treatment reduced R. solanacearum abundance in soil by 17.6% at pre-planting and 18.7% at 90 days before harvesting, but BV inoculation did not influence R. solanacearum abundance. ASD and ASD+BV treatments effectively reduced the occurrence of bacterial wilt, improved soil nutrient status and increased soil microbial activity at 90 days before harvesting. Principal co-ordinate analysis showed that the soil bacterial community was significantly influenced by ASD treatment both at pre-planting and at 90 days before harvesting. Further investigation found that ASD contributed to the enrichment of beneficial flora (Bacillus and Streptomyces). Moreover, pH was an important environmental factor affecting the abundance of R. solanacearum in soil. Co-occurrence network analysis showed that ASD treatment significantly increased network connection of bacterial communities and the proportion of beneficial microorganisms (Proteobacteria and Firmicutes), leading to complex soil bacterial co-occurrence networks both at pre-planting and at 90 days before harvesting. Collectively, these results indicate that ASD treatment, but not microbial inoculation can enhance tomato plant resistance to bacterial wilt by improving soil quality and modulating the soil bacterial community.

Keywords: Ralstonia solanacearum plant growth-promoting rhizobacteria anaerobic soil disinfestation soil quality soil microorganisms

Received: 18 March 2024 Accepted: 06 May 2024

Fund: This study was supported by the National Natural Science Foundation of China (31870420), and the Science and Technology Program of Guangdong Province, China (2121A0505030057).

About author: Taowen Pan, Mobile: +86-17728109913, E-mail: pantaowen123@126.com; #Correspondence Kunzheng Cai, Mobile: +86-13672408736, E-mail: kzcai@scau.edu.cn

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Taowen Pan, Yulin Chen, Sicong Li, Lei Wang, Joji Muramoto, Carol Shennan, Jihui Tian, Kunzheng Cai. 2025. Anaerobic soil disinfestation rather than Bacillus velezensis Y6 inoculant suppresses tomato bacterial wilt by improving soil quality and manipulating bacterial communities. Journal of Integrative Agriculture, 24(2): 754-768.

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