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Soil Acidification Aggravates the Occurrence of Bacterial Wilt in South China.

ABSTRACT: Soil acidification is a major problem in modern agricultural systems and is an important factor affecting the soil microbial community and soil health. However, little is known about the effect of soil acidification on soil-borne plant diseases. We performed a 4-year investigation in South China to evaluate the correlation between soil acidification and the occurrence of bacterial wilt. The results showed that the average soil pH in fields infected by bacterial wilt disease was much lower than that in non-disease fields. Moreover, the proportion of infected soils with pH lower than 5.5 was much higher than that of non-infected soils, and this phenomenon became more obvious as the area of bacterial wilt disease increased at soil pH lower than 5.5 from 2011 to 2014. Then, in a field pot experiment, bacterial wilt disease developed more quickly and severely in acidic conditions of pH 4.5, 5.0, and 5.5. These results indicate that soil acidification can cause the outbreak of bacterial wilt disease. Further experiments showed that acidic conditions (pH 4.5-5.5) favored the growth of the pathogen Ralstonia solanacearum but suppressed the growth and antagonistic activity of antagonistic bacteria of Pseudomonas fluorescens and Bacillus cereus. Moreover, acidic conditions of pH 5.5 were conducive to the expression of the virulence genes PopA, PrhA, and SolR but restrained resistance gene expression in tobacco. Finally, application of wood ash and lime as soil pH amendments improved soil pH and reduced the occurrence of bacterial wilt. Together, these findings improve our understanding of the correlation between soil acidification and soil-borne plant diseases and also suggest that regulation of soil acidification is the precondition and foundation of controlling bacterial wilt.

SUBMITTER: Li S

PROVIDER: S-EPMC5403937 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Bacterial wilt is accompanied by microbial communities shift and soil acidification. However, the relationship between the changes of bacterial communities and bacterial wilt under the influence of different acidification levels has not been fully elucidated. Here, we analyzed the abundance of Ralstonia solanacearum, rhizosphere bacterial communities and carbon metabolism at differently acidic levels (pH 6.45, pH 5.60, pH 5.35, pH 4.90 and pH 4.45) and soil amendment treatment (CaO). The results indicated that both the abundance of R. solanacearum and the incidence of bacterial wilt showed a significant trend of first increasing and then decreasing with the increase of soil pH. The Firmicutes phylum and potentially beneficial genera Bacillus, Paenibacillus, Flavobacterium and Pseudomonas were significantly enriched at pH 6.45. The metabolic ability in response to the l-arginine and 4-hydroxybenzoic acid was significantly increased at pH 6.45. After using CaO to increase the pH of diseased soil from 5.45 to 6.05, the abundance of R. solanacearum and the incidence of bacterial wilt were significantly reduced, the Firmicutes and potentially beneficial genera Bacillus and Pseudomonas were significantly enriched. Overall, alleviating soil acidification to a slightly acidic level (pH 6.0-6.5) could suppress bacterial wilt by suppressing the growth of R. solanacearum and enriching the rhizosphere potentially beneficial bacteria, and further emphasized the importance of increasing soil pH in biological control of bacterial wilt. IMPORTANCE The rhizosphere microbiota and soil acidification have been shown to have impacts on bacterial wilt. However, the influence of different acidification levels on the rhizosphere communities and bacterial wilt has not been fully studied. In this study, the potentially beneficial bacteria (Bacillus and Pseudomonas) were significantly enriched in the slightly acidic soil (pH 6.45), leading to the increase of the metabolism of 4-hydroxybenzoic acid and the decrease of pathogenic R. solanacearum, thereby alleviating the occurrence of bacterial wilt. The changes of potentially beneficial bacteria and pathogenic R. solanacearum in strongly acidic soil (pH 5.35) with the highest incidence of bacterial wilt were just the opposite. These findings help clarify the mechanisms by which soil bacteria exert influence on bacterial wilt outbreak under different soil acidification levels.

Project description:Bacterial wilt disease is a devastating disease of crops, which leads to huge economic loss worldwide. It is hypothesized that the occurrence of bacterial wilt may be related to changes in soil chemical properties and microbial interactions. In this study, we compared the soil chemical properties and microbial network structures of a healthy soil (HS) and a bacterial wilt-susceptible soil (BWS). The contents of available nitrogen, potassium, and phosphorus and the soil pH in the BWS were significantly lower than those in the HS. BWS showed nutrient deficiency and acidification in comparison with the HS. The structure and composition of the BWS network were quite different from those of the HS network. The BWS network had fewer modules and edges and lower connectivity than the HS network. The HS network contained more interacting species, more key microorganisms, and better high-order organization and thus was more complex and stable than the BWS network. Most nodes and module memberships were unshared by the two networks, while the ones that were shared showed different topological roles. Some generalists in the HS network became specialists in the BWS network, indicating that the topological roles of microbes were changed and key microorganisms were shifted in the BWS. In summary, the composition and structure of the microbial network of the BWS were different from that of the HS. Many microbial network connections were missing in the BWS, which most likely provided conditions leading to higher rates of bacterial wilt disease.IMPORTANCE Bacterial wilt disease is caused by the pathogen Ralstonia solanacearum and is a widespread devastating soilborne disease leading to huge economic losses worldwide. The soil microbial community is crucial to the capacity of soils to suppress soilborne diseases through complex interactions. Network analysis can effectively explore these complex interactions. In this study, we used a random matrix theory (RMT)-based network approach to investigate the changes in microbial network and associated microbial interactions in a bacterial wilt-susceptible soil (BWS) in comparison to a healthy soil (HS). We found that the structure and composition of the microbial network in BWSs were quite different from those of the HS. The BWS network had fewer modules, edges, and key microorganisms and lower connectivity than the HS network. In the BWSs, apparently the topological role of microbes was changed and key microorganisms were shifted to specialists.

Project description:BackgroundBacterial viruses, phages, play a key role in nutrient turnover and lysis of bacteria in terrestrial ecosystems. While phages are abundant in soils, their effects on plant pathogens and rhizosphere bacterial communities are poorly understood. Here, we used metagenomics and direct experiments to causally test if differences in rhizosphere phage communities could explain variation in soil suppressiveness and bacterial wilt plant disease outcomes by plant-pathogenic Ralstonia solanacearum bacterium. Specifically, we tested two hypotheses: (1) that healthy plants are associated with stronger top-down pathogen control by R. solanacearum-specific phages (i.e. 'primary phages') and (2) that 'secondary phages' that target pathogen-inhibiting bacteria play a stronger role in diseased plant rhizosphere microbiomes by indirectly 'helping' the pathogen.ResultsUsing a repeated sampling of tomato rhizosphere soil in the field, we show that healthy plants are associated with distinct phage communities that contain relatively higher abundances of R. solanacearum-specific phages that exert strong top-down pathogen density control. Moreover, 'secondary phages' that targeted pathogen-inhibiting bacteria were more abundant in the diseased plant microbiomes. The roles of R. solanacearum-specific and 'secondary phages' were directly validated in separate greenhouse experiments where we causally show that phages can reduce soil suppressiveness, both directly and indirectly, via top-down control of pathogen densities and by alleviating interference competition between pathogen-inhibiting bacteria and the pathogen.ConclusionsTogether, our findings demonstrate that soil suppressiveness, which is most often attributed to bacteria, could be driven by rhizosphere phage communities that regulate R. solanacearum densities and strength of interference competition with pathogen-suppressing bacteria. Rhizosphere phage communities are hence likely to be important in determining bacterial wilt disease outcomes and soil suppressiveness in agricultural fields. Video Abstract.

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Soil Acidification Aggravates the Occurrence of Bacterial Wilt in South China.

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