What role do biocontrol agents with Mg2+ play in the fate of antibiotic resistome and pathogenic bacteria in the phyllosphere?

The contamination of the plant phyllosphere with antibiotics and antibiotic resistance genes (ARGs), caused by application of antibiotics, is a significant environmental issue in agricultural management. Alternatively, biocontrol agents are environmentally friendly and have attracted a lot of interest. However, the influence of biocontrol agents on the phyllosphere resistome remains unknown. In this study, we applied biocontrol agents to control the wildfire disease in the Solanaceae crops and investigated their effects on the resistome and the pathogen in the phyllosphere by using metagenomics. A total of 250 ARGs were detected from 15 samples, which showed a variation in distribution across treatments of biocontrol agents (BA), BA with Mg2+ (T1), BA with Mn2+ (T2), and kasugamycin (T3) and nontreated (CK). The results showed that the abundance of ARGs under the treatment of BA-Mg2+ was lower than that in the CK group. The abundance of cphA3 (carbapenem resistance), PME-1 (carbapenem resistance), tcr3 (tetracycline antibiotic resistance), and AAC (3)-VIIIa (aminoglycoside antibiotic resistance) in BA-Mg2+ was significantly higher than that in BA-Mn2+ (P < 0.05). The abundance of cphA3, PME_1, and tcr3 was significantly negatively related to the abundance of the phyllosphere pathogen Pseudomonas syringae (P < 0.05). We also found that the upstream and downstream regions of cphA3 were relatively conserved, in which rpl, rpm, and rps gene families were identified in most sequences (92%). The Ka/Ks of cphA3 was 0 in all observed sequences, indicating that under the action of purifying selection, nonsynonymous substitutions are often gradually eliminated in the population. Overall, this study clarifies the effect of biocontrol agents with Mg2+ on the distribution of the phyllosphere resistome and provides evolutionary insights into the biocontrol process. IMPORTANCE: Our study applied metagenomics analysis to examine the impact of biocontrol agents (BAs) on the phyllosphere resistome and the pathogen. Irregular use of antibiotics has led to the escalating dissemination of antibiotic resistance genes (ARGs) in the environment. The majority of BA research has focused on the effect of monospecies on the plant disease control process, the role of the compound BA with nutrition elements in the phyllosphere disease, and the resistome is still unknown. We believe BAs are eco-friendly alternatives for antibiotics to combat the transfer of ARGs. Our results revealed that BA-Mg2+ had a lower relative abundance of ARGs compared to the CK group, and the phyllosphere pathogen Pseudomonas syringae was negatively related to three specific ARGs, cphA3, PME-1, and tcr3. These three genes also present different Ka/Ks. We believe that the identification of the distribution and evolution modes of ARGs further elucidates the ecological role and facilitates the development of BAs, which will attract general interest in this field.

Enhancing plant growth in biofertilizer-amended soil through nitrogen-transforming microbial communities.

Biofertilizers have immense potential for enhancing agricultural productivity. However, there is still a need for clarification regarding the specific mechanisms through which these biofertilizers improve soil properties and stimulate plant growth. In this research, a bacterial agent was utilized to enhance plant growth and investigate the microbial modulation mechanism of soil nutrient turnover using metagenomic technology. The results demonstrated a significant increase in soil fast-acting nitrogen (by 46.7%) and fast-acting phosphorus (by 88.6%) upon application of the bacterial agent. This finding suggests that stimulated soil microbes contribute to enhanced nutrient transformation, ultimately leading to improved plant growth. Furthermore, the application of the bacterial agent had a notable impact on the accumulation of key genes involved in nitrogen cycling. Notably, it enhanced nitrification genes (amo, hao, and nar), while denitrification genes (nir and nor) showed a slight decrease. This indicates that ammonium oxidation may be the primary pathway for increasing fast-acting nitrogen in soils. Additionally, the bacterial agent influenced the composition and functional structure of the soil microbial community. Moreover, the metagenome-assembled genomes (MAGs) obtained from the soil microbial communities exhibited complementary metabolic processes, suggesting mutual nutrient exchange. These MAGs contained widely distributed and highly abundant genes encoding plant growth promotion (PGP) traits. These findings emphasize how soil microbial communities can enhance vegetation growth by increasing nutrient availability and regulating plant hormone production. This effect can be further enhanced by introducing inoculated microbial agents. In conclusion, this study provides novel insights into the mechanisms underlying the beneficial effects of biofertilizers on soil properties and plant growth. The significant increase in nutrient availability, modulation of key genes involved in nitrogen cycling, and the presence of MAGs encoding PGP traits highlight the potential of biofertilizers to improve agricultural practices. These findings have important implications for enhancing agricultural sustainability and productivity, with positive societal and environmental impacts.

Influence of Association Network Properties and Ecological Assembly of the Foliar Fugal Community on Crop Quality.

Revealing community assembly and their impacts on ecosystem service is a core issue in microbial ecology. However, what ecological factors play dominant roles in phyllosphere fungal community assembly and how they link to crop quality are largely unknown. Here, we applied internal transcriptional spacer high-throughput sequencing to investigate foliar fungal community assembly across three cultivars of a Solanaceae crop (tobacco) and two planting regions with different climatic conditions. Network analyses were used to reveal the pattern in foliar fungal co-occurrence, and phylogenetic null model analysis was used to elucidate the ecological assembly of foliar fungal communities. We found that the sensory quality of crop leaves and the composition of foliar fungal community varied significantly across planting regions and cultivars. In Guangcun (GC), a region with relatively high humidity and low precipitation, there was a higher diversity and more unique fungal species than the region of Wuzhishan (WZS). Further, we found that the association network of foliar fungal communities in GC was more complex than that in WZS, and the network properties were closely related to the sensory quality of crop. Finally, the results of the phylogenetic analyses show that the stochastic processes played important roles in the foliar fungal community assembly, and their relative importance was significantly correlated with the sensory quality of crop leaves, which implies that ecological assembly processes could affect crop quality. Taken together, our results highlight that climatic conditions, and plant cultivars play key roles in the assembly of foliar fungal communities and crop quality, which enhances our understanding of the connections between the phyllosphere microbiome and ecosystem services, especially in agricultural production.