Ralstonia solanacearum pathogen disrupts bacterial rhizosphere microbiome during an invasion

Abstract

Plant pathogen invasions are often associated with changes in physical environmental conditions and the composition of host-associated rhizosphere microbiome. It is however unclear how these factors interact and correlate with each other in determining plant disease dynamics in natural field conditions. To study this, we temporally sampled the rhizosphere of tomato plants that were exposed to moderate to aggressive Ralstonia solanacearum pathogen invasions over one crop season. We found that physiochemical soil properties correlated weakly with the severity of pathogen invasion apart from the water-soluble nitrogen concentration, which increased more clearly during the aggressive invasion. Instead, a much stronger link was found between pathogen invasion and reduced abundance and diversity of various rhizosphere bacterial taxa, simplification of bacterial interaction networks and loss of several predicted functional genes. We further verified our results in a separate greenhouse experiment to show that pathogen invasion causally drives similar changes in rhizosphere microbiome diversity and composition under controlled environmental conditions. Our results suggest that R. solanacearum invasion disrupts rhizosphere bacterial communities leading to clear reduction in the diversity and abundance of non-pathogenic bacteria. These changes could potentially affect the likelihood of secondary pathogen invasions during following crop seasons as less diverse microbial communities are also often less resistant to invasions. Strong negative correlation between pathogen and non-pathogenic bacterial densities further suggest that relative pathogen abundance could better predict the severity of bacterial wilt disease outbreaks compared to absolute pathogen abundance. Monitoring the dynamics of whole microbiomes could thus open new avenues for more accurate disease diagnostics in the future.

High abundance of Ralstonia solanacearum changed tomato rhizosphere microbiome and metabolome

“…Generally, the low microbial diversity in the rhizosphere soil is beneficial for the pathogen invasion [24]. Indeed, in our study the success of pathogen invasion decreased the microbial diversity as shown by the significant decrease in Shannon, Chao and Faith's PD indexes at high RS abundance samples, which indicated that pathogen invasion disrupted the host associated microbiome [43]. Principal coordinates analysis showed that the alteration of pathogen abundance altered the composition of bacterial community, and analysis after removing OTU of RS further supported this conclusion.…”

“…Species invasion has a strong impact on the original ecosystem through competition of resources and niches with the indigenous microbes [43]. In rhizosphere soil, pathogen invasion can also affect the microbial community by indirectly influencing the host [38,41], for example, Berendsen et al [4] showed that Arabidopsis thaliana specifically promotes three bacterial species in the rhizosphere upon foliar defense activation by the downy mildew pathogen Hyaloperonospora arabidopsidis.…”

Relationships between community composition, productivity and invasion resistance in semi-natural bacterial microcosms

“…Community cell yield has been neglected in favour of hypotheses about diversity and composition in microbial invasion ecology -even though it has long been understood that the effects of composition often manifest as productivity, driving differences in invasion resistance [11,22,25,26]. The most adept microbial invaders have often evolved to exploit this as exemplified by the triggering of inflammation to reduce the density of resident competitors by invading pathogens of the gut [7] and reductions of antagonistic populations during Ralstonia invasion into the rhizosphere [49]. Furthermore, in natural systems, community cell yield may play an even more central role, with short-term disturbances opening the door for invaders unless communities are able to quickly recover to carrying capacity [24].…”

“…Resident microbial communities can constrain invasions by competing for resources, by producing antimicrobial compounds, or by otherwise altering environmental conditions that are unfavourable to the invader (e.g. through production of inhibitory substances) [21,36,37,49]. Conversely, resident microbial communities might facilitate invasions by producing resources that would otherwise be unavailable, or by favourably altering the environment [22,36].…”

The phenotype and pathogenicity of Ralstonia solanacearum transformed under prolonged stress of excessive exogenous nitrogen

“…Recent research about nitrogen on plant pathogens mainly focused on the effect of nitrogen application on soil microbial community structure in the field (Wang, Xiao, et al, ). The concentration of water‐soluble nitrogen in soil correlated strongly with the aggressive invasion of soil pathogens (Wei et al, ). A previous report showed that when 1 mol of ammonium ion was absorbed in soil, two moles of hydrogen ions were released (Wang, Zhang, Zhao, & Xu, ; Wang, Xiao, et al, ).…”