The phyllosphere and soil are dynamic habitats for microbial communities. Non-pathogenic microbiota, including leaf and soil beneficial bacteria, plays a crucial role in plant growth and health, as well as in soil fertility and organic matter production. In sustainable agriculture, it is important to understand the composition of these bacterial communities, their changes in response to disturbances, and their resilience to agricultural practices. Widespread pesticide application may have had non-target impacts on these beneficial microorganisms. Neonicotinoids are a family of systemic insecticides being vastly used to control soil and foliar pests in recent decades. A few studies have demonstrated the long-term and non-target effects of neonicotinoids on agroecosystem microbiota, but the generality of these findings remains unclear. In this study, we used 16S rRNA gene amplicon sequencing to characterize the effects of neonicotinoid seed treatment on soil and phyllosphere bacterial community diversity, composition and temporal dynamics in a 3-year soybean/corn rotation in Quebec, Canada. We found that habitat, host species and time are stronger drivers of variation in bacterial composition than neonicotinoid application. They, respectively, explained 37.3, 3.2, and 2.9% of the community variation. However, neonicotinoids did have an impact on bacterial community structure, especially on the taxonomic composition of soil communities (2.6%) and over time (2.4%). They also caused a decrease in soil alpha diversity in the middle of the growing season. While the neonicotinoid treatment favored some bacterial genera known as neonicotinoid biodegraders, there was a decline in the relative abundance of some potentially beneficial soil bacteria in response to the pesticide application. Some of these bacteria, such as the plant growth-promoting rhizobacteria and the bacteria involved in the nitrogen cycle, are vital for plant growth and improve soil fertility. Overall, our results indicate that neonicotinoids have non-target effects on phyllosphere and soil bacterial communities in a soybean-corn agroecosystem. Exploring the interactions among bacteria and other organisms, as well as the bacterial functional responses to the pesticide treatment, may enhance our understanding of these non-target effects and help us adapt agricultural practices to control these impacts.

No abstract

Neonicotinoids, a class of systemic insecticides, have been widely used for decades against various insect pests. Past studies have reported non-target effects of neonicotinoids on some beneficial macro- and micro-organisms. Given the crucial role that the soil microbiota plays in sustaining soil fertility, it is critical to understand how microbial taxonomic composition and gene expression respond to neonicotinoid exposure. To date, few studies have focused on this question, and these studies have evaluated the shifts in soil microbial taxonomic composition or used soil biochemical analyses to assess the changes in microbial functions. In this study, we have applied a metatranscriptomic approach to quantify the variability in soil microbial gene expression in a two-year soybean/corn crop rotation in Quebec, Canada. We identified weak and temporally inconsistent effects of neonicotinoid application on soil microbial gene expression, as well as a strong temporal variation in soil microbial gene expression among months and years. Neonicotinoid seed treatment altered the expression of a small number of microbial genes, including genes associated with heat shock proteins, regulatory functions, metabolic processes and DNA repair. These changes in gene expression varied during the growing season and between years. Overall, the composition of soil microbial expressed genes seems to be more resilient and less affected by neonicotinoid application than soil microbial taxonomic composition. Our study is among the first to document the effects of neonicotinoid seed treatment on microbial gene expression and highlights the strong temporal variability of soil microbial gene expression and its responses to neonicotinoid seed treatments.

BackgroundThe phyllosphere and soil are dynamic habitats for microbial communities. Non-pathogenic microbiota, including leaf and soil beneficial bacteria, plays a crucial role in plant growth and health, as well as in soil fertility and organic matter production. In sustainable agriculture, it is important to understand the composition of these bacterial communities, their changes in response to disturbances, and their resilience to agricultural practices. Widespread pesticide application may have had non-target impacts on these beneficial microorganisms. Neonicotinoids are a family of systemic insecticides being vastly used to control soil and foliar pests in recent decades. A few studies have demonstrated the long-term and non-target effects of neonicotinoids on agroecosystem microbiota, but the generality of these findings remains unclear. In this study, we used 16S rRNA gene amplicon sequencing to characterize the effects of neonicotinoid seed treatment on soil and phyllosphere bacterial community diversity, composition and temporal dynamics in a three-year soybean/corn rotation in Quebec, Canada. Results We found that habitat, host species and time are stronger drivers of variation in bacterial composition than neonicotinoid application. They respectively explained 37.3%, 3.2% and 2.9% of the community variation. However, neonicotinoids did have an impact on bacterial community structure, especially on the taxonomic composition of soil communities (2.6%) and over time (2.4%). They also caused a decrease in soil alpha diversity in the middle of the growing season. While the neonicotinoid treatment favored some bacterial genera known as neonicotinoid biodegraders, there was a decline in the relative abundance of some potentially beneficial soil bacteria, such as the plant growth-promoting rhizobacteria and the bacteria involved in the nitrogen cycle, in response to the pesticide application.ConclusionsOur results indicate that neonicotinoids have non-target effects on phyllosphere and soil bacterial communities in a soybean-corn agroecosystem, especially potentially beneficial bacteria that are vital for plant growth and improve soil fertility. Exploring the interactions among bacteria and other organisms, as well as the bacterial functional responses to the pesticide treatment, may enhance our understanding of these non-target effects and help us adapt agricultural practices to control these impacts.

Neonicotinoids, a class of systemic insecticides, have been widely used for decades against various insect pests. Previous studies have reported non-target effects of neonicotinoids on some beneficial macro- and micro-organisms. Considering the crucial role the soil microbiota plays in sustaining soil fertility, it is critical to understand how neonicotinoid exposure affects the microbial taxonomic composition and gene expression. However, most studies to date have evaluated soil microbial taxonomic compositions or assessed microbial functions based on soil biochemical analysis. In this study, we have applied a metatranscriptomic approach to quantify the variability in soil microbial gene expression in a 2 year soybean/corn crop rotation in Quebec, Canada. We identified weak and temporally inconsistent effects of neonicotinoid application on soil microbial gene expression, as well as a strong temporal variation in soil microbial gene expression among months and years. Neonicotinoid seed treatment altered the expression of a small number of microbial genes, including genes associated with heat shock proteins, regulatory functions, metabolic processes and DNA repair. These changes in gene expression varied during the growing season and between years. Overall, the composition of soil microbial expressed genes seems to be more resilient and less affected by neonicotinoid application than soil microbial taxonomic composition. Our study is among the first to document the effects of neonicotinoid seed treatment on microbial gene expression and highlights the strong temporal variability of soil microbial gene expression and its responses to neonicotinoid seed treatments.

No abstract

Neonicotinoid insecticides are widely used to control early-season and foliar-feeding pests. Some studies have revealed their non-target impacts on pollinators and other invertebrates, but few investigated their effects on soil microbiota. Given the crucial role of soil prokaryotic and eukaryotic microbial communities in agroecosystem regulation and their contribution to soil fertility, it is critical to understand their structure and changes in response to disturbances such as pesticide application. Among these communities, free-living nematodes have the potential to indicate the ecological changes in soil caused by environmental stress and have a key role in forming and modulating soil microbial composition and function by feeding on other soil microorganisms or interacting with them. Here, we used 18S rRNA gene amplicon sequencing to characterize the effects of neonicotinoids on soil nematode communities in a three-year soybean/corn crop rotation in Quebec, Canada. We also quantified the changes in nematode-bacteria co-occurrence networks in soil exposed to neonicotinoids. We found that neonicotinoid seed treatment significantly explained variation in nematode community composition and affected the relative abundance of some nematode families, such as a decrease in the omnivorous family Dorylaimidae in neonicotinoid-treated samples. Moreover, neonicotinoids altered the patterns of nematode-bacteria co-occurrence, including the structure and taxonomic composition of the networks. However, it is unclear whether neonicotinoids affected bacterial co-occurrence networks directly or indirectly by affecting nematodes that feed on bacteria. Further research is needed to understand how neonicotinoids affect nematodes and the role of nematodes in microbial network variation in soil exposed to neonicotinoids.