Neonicotinoid Seed Treatments Have Significant Non-target Effects on Phyllosphere and Soil Bacterial Communities

Abstract

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.

Effects of Neonicotinoid Seed Treatments on Soil Microbial Gene Expression Vary with Time in an Agricultural Ecosystem

“…Overall, despite our hypothesis that the expression of pesticide degradation-related genes would increase and the expression of nitrification-related genes decrease in response to neonicotinoid seed treatment, and previous observations of soil microbial taxonomic and physiochemical changes due to neonicotinoid application (58,31,40,22,25), we did not detect any significant shifts in the expression of genes related to biodegradation of neonicotinoids or any decline in the expression of the genes associated with nitrification. We suggest several possible explanations for this finding: First, as mentioned previously, strong temporal changes in the expression of soil microbial genes may have masked subtle effects of neonicotinoid seed treatments on gene expression.…”

“…Neonicotinoid seed treatment had weak and temporally variable effects on soil microbial gene expression in a soybean-corn agroecosystem. Conversely, time was a strong driver of the composition and diversity of soil microbial expressed genes, as expected and similar to its important effects on soil microbial taxonomic composition and diversity (44,25). Time had a very strong effect on the expression of numerous soil microbial genes.…”

“…Our results thus suggest that while gene expression in soil microbial communities is highly variable in time, these communities are either highly resistant or resilient to changes in gene expression in response to neonicotinoid seed treatment. This can be due to functional redundancy in the identity of expressed genes, despite the major variation in the taxonomic composition of these microbial communities that we have previously observed (25). Past studies have suggested that various co-occurred microbial communities may be functionally redundant.…”

“…Finally, it is possible that soil microbial communities are functionally resistant or resilient, leading to few changes in gene expression in response to neonicotinoid seed treatment. Compared s Submission Template mSystems Submission Template mSystems Submission Template mSystems Submission Template mSystems Submission Template mSystems Submission Te to measures of soil microbial community taxonomic structure (25), soil microbial gene expression seems to be less sensitive to the stress imposed by neonicotinoid application. This is probably due to the functional resilience and redundancy of microbial communities (59), and it is in line with the findings of previous studies showing less variability in microbial gene expression than taxonomic composition (49,50,52,60,54).…”

“…Neonicotinoids are supposed to be selectively more toxic to invertebrates because of the fundamental distinctions between their nicotinic acetylcholine receptors (nAChRs) compared to vertebrates (9). However, non-target impacts of these pesticides on the taxonomic composition of soil microbial communities have been documented, including shifts in the abundance of diverse taxa, such as a decrease in bacteria genera involved in nitrification and an increase in bacteria genera related to neonicotinoid biodegradation (19,20,21,22,23,24,25). An increase in the abundance of the genes coding for the cytochrome P450 enzyme family has been reported in response to neonicotinoid exposure, based on soil microbial amplicon and metagenomic sequencing (26,27).…”