Plant-beneficial bacterial inoculants are of great interest in agriculture as they have the potential to promote plant growth and health. However, the inoculation of the rhizosphere microbiome often results in a suboptimal or transient colonization, which is due to a variety of factors that influence the fate of the inoculant. To better understand the fate of plant-beneficial inoculants in complex rhizosphere microbiomes, composed by hundreds of genotypes and multifactorial selection mechanisms, controlled studies with high-complexity soil microbiomes are needed.We analysed early compositional changes in a taxa-rich natural soil bacterial community under both exponential nutrient-rich and stationary nutrient-limited growth conditions (i.e. growing and stable communities, respectively) following inoculation with the plant-beneficial bacterium Pseudomonas protegens in a bulk soil or a wheat rhizosphere environment. P. protegens successfully established under all conditions tested and was more abundant in the rhizosphere of the stable community. Nutrient availability was a major factor driving microbiome composition and structure as well as the underlying assembly processes. While access to nutrients resulted in communities assembled mainly by homogeneous selection, stochastic processes dominated under the nutrient-deprived conditions. We also observed an increased rhizosphere selection effect under nutrient-limited conditions, resulting in a higher number of amplicon sequence variants (ASVs) whose relative abundance was enriched. The inoculation with P. protegens produced discrete changes, some of which involved other Pseudomonas. Direct competition between Pseudomonas strains partially failed to replicate the observed differences in the microbiome and pointed to a more complex interaction network.The results of this study show that nutrient availability is a major driving force of microbiome composition, structure and diversity in both the bulk soil and the wheat rhizosphere and determines the assembly processes that govern early microbiome development. The successful establishment of the inoculant was facilitated by the wheat rhizosphere and produced discrete changes among other members of the microbiome. Direct competition between Pseudomonas strains only partially explained the microbiome changes, indicating that indirect interactions or spatial distribution in the rhizosphere or soil interface may be crucial for the survival of certain bacteria. Video Abstract. 

Changes in structure and assembly of a species-rich soil natural community with contrasting nutrient availability upon establishment of a plant-beneficial Pseudomonas in the wheat rhizosphere

Viruses, with an estimated abundance of 1031 on Earth, are an important component of soil ecosystems. As obligate parasites that entirely depend on hosts for reproduction and survival, viruses have been linked to microbial community diversity and metabolic activities in soil. Emerging evidence indicates that soil viruses influence a broad-spectrum of processes that sustain soil biodiversity, biogeochemical cycling, fertility, and plant health. Research on soil viruses is in its early stages. Even observational assessments of viral ecology such as abundance, diversity, distribution, life strategies, ecological relevance, and functions, are only just beginning to be revealed. In this review, we summarize the state of knowledge concerning the potential function(s) of soil viruses and how they likely influence microbial community composition, nutrient cycles, and carbon dynamics for example. As major drivers of microbial mortality and functioning across a wide range of spatial and temporal scales, soil viruses appear to be key regulators of cellular metabolism and microbial community properties and as well as biogeochemical processes critical to ecosystem function. We conclude that soil viruses are an indispensable component of soil ecology demanding further investigation. Defining abiotic interactions of viruses within the soil environment, revealing the virus-host interaction networks, and elucidating the roles of soil viruses in carbon and nutrient cycling are but a few of the many aspects of soil viral ecology worthy of future investigation. A more complete view of viral participation in soil food webs in the face of a changing climate will lead to improved management of soil ecosystem services and environmental sustainability. 

Incorporating viruses into soil ecology: A new dimension to understand biogeochemical cycling

Activated sludge (AS) systems in wastewater treatment plants (WWTPs) harbor enormous viruses that regulate microbial metabolism and nutrient cycling, significantly influencing the stability of AS systems. However, our knowledge about the diversity of viral taxonomic groups and functional traits in global AS systems is still limited. To address this gap, we investigated the global diversity and biogeography of DNA viral communities in AS systems using 85,114 viral operational taxonomic units (vOTUs) recovered from 144 AS samples collected across 54 WWTPs from 13 different countries.AS viral communities and their functional traits exhibited distance-decay relationship (DDR) at the global scale and latitudinal diversity gradient (LDG) from equator to mid-latitude. Furthermore, it was observed that AS viral community and functional gene structures were largely driven by the geographic factors and wastewater types, of which the geographic factors were more important. Carrying and disseminating auxiliary metabolic genes (AMGs) associated with the degradation of polysaccharides, sulfate reduction, denitrification, and organic phosphoester hydrolysis, as well as the lysis of crucial functional microbes that govern biogeochemical cycles were two major ways by which viruses could regulate AS functions. It was worth noting that our study revealed a high abundance of antibiotic resistance genes (ARGs) in viral genomes, suggesting that viruses were key reservoirs of ARGs in AS systems.Our results demonstrated the highly diverse taxonomic groups and functional traits of viruses in AS systems. Viral lysis of host microbes and virus-mediated HGT can regulate the biogeochemical and nutrient cycles, thus affecting the performance of AS systems. These findings provide important insights into the viral diversity, function, and ecology in AS systems on a global scale. Video Abstract. 

Global diversity and biogeography of DNA viral communities in activated sludge systems

Viruses, as the most abundant organisms, significantly influence ecological function and microbial survival in soils, yet little was known about how viruses and virus-microbe interactions respond to environmental stresses induced by metal(loid) contaminations. Here, we conducted the metagenomic analysis to investigate the adaptative mechanisms of soil viruses under different metal(loid) contamination levels. By capturing a catalogue of 23,066 viruses, we found that viral communities exhibited the increased richness, diversity, and the temperate to lytic ratio in facing the highest metal(loid) contaminations. Meanwhile, viruses displayed obvious lineage-specific infection modes to distinct dominant hosts under different pollution levels. Viral functions linking to the inhibition of transcription and the enhancement of DNA repairment as well as multiple resistance not only contributed to coping with elevated multiple metal(loid) stresses, but also facilitated the adaptation and functioning of viral hosts. Moreover, the harmonious coexistence of viruses and resistant/pathogenic bacteria under the heaviest contaminations potentially exacerbated disseminating resistance and pathogenicity, while viruses under the lightest contaminations might be natural predators of resistant/pathogenic bacteria through lysing host cells. Overall, this study highlights the ecological importance of viral adaptation and the interactions between viruses and resistant/pathogenic bacteria in contaminated environments, contributing to developing virus-based approaches to soil restoration. 

Distinct adaptive strategies and microbial interactions of soil viruses under different metal(loid) contaminations.

ABSTRACT Agroecological management of infectious crop diseases represents a challenge due to the complexity of the ecological processes involved, the great variety of plant pathogens, and the ecological and socio-cultural particularities of agroecosystems. As general management strategies, agroecology proposes the promotion of soil health, the diversification of vegetation, and a greater landscape heterogeneity. To prevent diseases, it is also necessary to consider specific practices for these organisms, (i.e. genetic resistance, seed treatments, crop microclimate management). In this article, we review the main contributions to agroecological management of diseases caused by fungi, bacteria, and viruses, including the literature on ecology of plant pathogens and holistic approaches that consider social processes. We start from a critique of integrated management and propose to broaden the disease triangle considering the biological interactions with plants, animals, microorganisms and the holobiont (plant and its microbiomes). We review how general strategies and specific disease management practices affect the different functional groups of plant pathogens, understood as a community. Finally, we emphasize that the objective from an agroecological viewpoint is to promote healthy crops. For this it is essential a holistic approach that considers the socio-economic context of farmers, values local knowledge and promotes collaborative social networks. GRAPHICAL ABSTRACT

Agroecological management of crop diseases: a review

Abstract Background Bacterial 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. Results Using 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. Conclusions Together, 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. 

/pdf/rhizosphere-phage-communities-drive-soil-suppressiveness-to-2dhx2qwh.pdf

Rhizosphere phage communities drive soil suppressiveness to bacterial wilt disease


 While temperature has been shown to affect the survival and growth of bacteria and their phage parasites, it is unclear if trade-offs between phage resistance and other bacterial traits depend on the temperature. Here, we experimentally compared the evolution of phage resistance–virulence trade-offs and underlying molecular mechanisms in phytopathogenic Ralstonia solanacearum bacterium at 25 °C and 35 °C temperature environments. We found that while phages reduced R. solanacearum densities relatively more at 25 °C, no difference in the final level of phage resistance was observed between temperature treatments. Instead, small colony variants (SCVs) with increased growth rate and mutations in the quorum-sensing (QS) signaling receptor gene, phcS, evolved in both temperature treatments. Interestingly, SCVs were also phage-resistant and reached higher frequencies in the presence of phages. Evolving phage resistance was costly, resulting in reduced carrying capacity, biofilm formation, and virulence in planta, possibly due to loss of QS-mediated expression of key virulence genes. We also observed mucoid phage-resistant colonies that showed loss of virulence and reduced twitching motility likely due to parallel mutations in prepilin peptidase gene, pilD. Moreover, phage-resistant SCVs from 35 °C-phage treatment had parallel mutations in type II secretion system (T2SS) genes (gspE and gspF). Adsorption assays confirmed the role of pilD as a phage receptor, while no loss of adsorption was found with phcS or T2SS mutants, indicative of other downstream phage resistance mechanisms. Additional transcriptomic analysis revealed upregulation of CBASS and type I restriction-modification phage defense systems in response to phage exposure, which coincided with reduced expression of motility and virulence-associated genes, including pilD and type II and III secretion systems. Together, these results suggest that while phage resistance–virulence trade-offs are not affected by the growth temperature, they could be mediated through both pre- and postinfection phage resistance mechanisms.

Phage selection drives resistance–virulence trade-offs in Ralstonia solanacearum plant-pathogenic bacterium irrespective of the growth temperature

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Rhizosphere phage communities drive soil suppressiveness to bacterial wilt disease

Phage selection drives resistance–virulence trade-offs in Ralstonia solanacearum plant-pathogenic bacterium irrespective of the growth temperature