Abstract
BackgroundSoil is an important reservoir of antibiotic resistance genes (ARGs), but their potential risk in different ecosystems as well as response to anthropogenic land use change is unknown. We used a metagenomic approach and datasets with well-characterized metadata to investigate ARG types and amounts in soil DNA of three native ecosystems: Alaskan tundra, US Midwestern prairie, and Amazon rainforest, as well as the effect of conversion of the latter two to agriculture and pasture, respectively.ResultsHigh diversity (242 ARG subtypes) and abundance (0.184–0.242 ARG copies per 16S rRNA gene copy) were observed irrespective of ecosystem, with multidrug resistance and efflux pump the dominant class and mechanism. Ten regulatory genes were identified and they accounted for 13–35% of resistome abundances in soils, among them arlR, cpxR, ompR, vanR, and vanS were dominant and observed in all studied soils. We identified 55 non-regulatory ARGs shared by all 26 soil metagenomes of the three ecosystems, which accounted for more than 81% of non-regulatory resistome abundance. Proteobacteria, Firmicutes, and Actinobacteria were primary ARG hosts, 7 of 10 most abundant ARGs were found in all of them. No significant differences in both ARG diversity and abundance were observed between native prairie soil and adjacent long-term cultivated agriculture soil. We chose 12 clinically important ARGs to evaluate at the sequence level and found them to be distinct from those in human pathogens, and when assembled they were even more dissimilar. Significant correlation was found between bacterial community structure and resistome profile, suggesting that variance in resistome profile was mainly driven by the bacterial community composition.ConclusionsOur results identify candidate background ARGs (shared in all 26 soils), classify ARG hosts, quantify resistance classes, and provide quantitative and sequence information suggestive of very low risk but also revealing resistance gene variants that might emerge in the future.Aify4ac4FW_3-HKjdJXvGWVideo abstract
Highlights
Soil is an important reservoir of antibiotic resistance genes (ARGs), but their potential risk in different ecosystems as well as response to anthropogenic land use change is unknown
Understanding soil resistomes at a broad geographic scale and across major ecosystems, especially in native soils which have not been exposed to anthropogenic activities, can help better define the background levels and types of ARGs, which is essential for assessing the potential risk of new human activities
Detected ARGs and regulatory genes A total of 268 ARG subtypes potentially conferring resistance to 21 classes of antibiotics were detected in the soils, with most of them belonging to antibiotic deactivation (106 ARGs) and efflux pump (93 ARGs) mechanisms (Fig. 1)
Summary
Soil is an important reservoir of antibiotic resistance genes (ARGs), but their potential risk in different ecosystems as well as response to anthropogenic land use change is unknown. We used a metagenomic approach and datasets with well-characterized metadata to investigate ARG types and amounts in soil DNA of three native ecosystems: Alaskan tundra, US Midwestern prairie, and Amazon rainforest, as well as the effect of conversion of the latter two to agriculture and pasture, respectively. 100 years of continuous cultivation significantly changed microbial diversity and structure in a consistent though not major way in North American Midwest prairie soils [11]. Since land use change has been and continues to be the most extensive alteration of the terrestrial environment, its impact on the soil resistome is important to understand
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