Field-based evidence for the enrichment of intrinsic antibiotic resistome stimulated by plant-derived fertilizer in agricultural soil

Liu, Shihai; Han, Ziming; Zhu, Dong; L, Xin; Deng, Liujie; Yang, Min

doi:10.1016/j.jes.2022.08.009

Cited by 5 publications

(3 citation statements)

References 65 publications

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“…Antibiotic use in agriculture to increase crop productivity can prompt the emergence of antibiotic resistance in the pathogens, which may reduce the effectiveness of antimicrobial therapy for agriculture production ( 1 ). Agricultural soil is a natural reservoir that stores antibiotic resistance genes (ARGs) and antibiotic-resistant bacteria (ARB) from both native microbes and those introduced by anthropogenic activities ( 3 , 4 ). Besides, resistant bacteria can enter the plant root and migrate into the leaf and stem tissue, accelerating the spread of resistance genes in plants ( 1 ).…”

Section: Introductionmentioning

confidence: 99%

What role do biocontrol agents with Mg ²⁺ play in the fate of antibiotic resistome and pathogenic bacteria in the phyllosphere?

Zhi,

Tan,

et al. 2024

mSystems

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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 Mg 2+ (T1), BA with Mn 2+ (T2), and kasugamycin (T3) and nontreated (CK). The results showed that the abundance of ARGs under the treatment of BA-Mg 2+ 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-Mg 2+ was significantly higher than that in BA-Mn 2+ ( 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 Mg 2+ 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-Mg 2+ 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.

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Section: Introductionmentioning

confidence: 99%

What role do biocontrol agents with Mg ²⁺ play in the fate of antibiotic resistome and pathogenic bacteria in the phyllosphere?

Zhi,

Tan,

et al. 2024

mSystems

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“…More importantly, many scholars have reported that the application of manure not only leads to the enrichment of ARGs in soil, but also signi cantly increases the enrichment of ARGs in plants (SHIHAI L et al,2024).Planting vegetables in manure-amended soils may lead to an increase in the abundance and diversity of some ARGs in vegetables ready for retail on the market after harvest (XIAOTING F et al,2023; CAIXIA Z et al,2022).A variety of tetracycline resistance genes and MGEs with high relative abundance were detected in the endophytic bacteria of three kinds of vegetable leaves harvested in the vegetable eld with manure application. MGEs have a certain risk of promoting the migration and diffusion of ARGs in vegetable endophytic bacteria, which means that eating these vegetables raw may pose a threat to human health (Wang.,2021).Yin et aldetected 205 ARGs from the phyllosphere of six vegetables, among which multidrug resistance genes were the most abundant (YUE Y et al,2022).Chen et alshowed that long-term application of chicken manure as an organic fertilizer to irrigate farmland soil would signi cantly increase the abundance of ARGs in the phyllosphere, with the highest enrichment factor of 2638 times(CHEN Q-L et al.,2018).Therefore, raw vegetables may be a potential way for soil ARGs to enter the human body, and its migration and driving mechanism to the lower end of the food chain through horizontal transfer need to be further explored.…”

Section: Introductionmentioning

confidence: 99%

Fecal antibiotic resistance genes were transferred through the distribution of soil-lettuce-snail food chain

Zhang

Zhao

Chen

et al. 2023

Environ Sci Pollut Res

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Massive antibiotic resistance genes (ARG) were detected in the soil modi ed by manure, which may affect human life safety through the food chain. However, the transmission of ARGs through the soil-plant-animal food chain is still unclear. Therefore, this study used high-throughput quantitative PCR technology to explore the effects of pig manure application on ARGs and bacterial communities in soil, lettuce phyllosphere and snail excrement.The results showed that a total of 384 ARGs and 48 MEGs were detected in all samples after 75 days of incubation. The diversity of ARGs and MGEs in soil components increased signi cantly by 87.04%and 40%with the addition of pig manure. The absolute abundance of ARGs in the phyllosphere of lettuce was signi cantly higher than that of the control group, with a growth rate of 212.5%.Six common ARGs were detected between the three components of the fertilization group, indicating that there was internal transmission of fecal ARGs between the trophic levels of the food chain.Firmicutes and Proteobacteria were identi ed as the dominant host bacteria in the food chain system, which were more likely to be used as carriers of ARGs to promote the spread of resistance in the food chain.The results were used to evaluate the potential ecological risks of livestock and poultry manure and provide theoretical basis and scienti c support for the formulation of ARGs prevention and control policies.

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“…На антибиотикорезистентность бактерий в окружающей среде могут оказывать влияние такие физико-химические факторы, как температура, доступность кислорода, рН почвенного раствора, содержание солей и трофические характеристики почвы . Так, в недавних исследованиях показано, что удобрения растительного происхождения стимулируют в почве «внутреннюю» резистентность к антибиотикам за счет улучшения питания местных бактерий (Liu et al, 2024). Известно о повышении антибиотикоустойчивости вследствие загрязнения почвы соединениями аммония , меди (Berg et al, 2005; и тяжелых металлов .…”

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Spread of antibiotic-resistant actinobacteria in soils exposed to various types of anthropogenic impact

Shirokikh,

Gembitskaya,

Ashikhmina

2024

Povolžskij èkologičeskij žurnal

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The work investigated the spectra of resistance to a certain set of antibiotics and the frequency of occurrence of resistant strains among typical soil bacteria – actinomycetes. Equal samples of isolates from sod-podzolic soil were used, selected at sites typifying various types of economic activity, namely: the production areas of a plywood factory and a chemical plant, the territory of a medical institution, and a solid waste collection and storage site. A total of 58 isolates with features characteristic of actinomycetes of the genus Streptomyces of the sections Cinereus, Helvolo-Flavus and Albus were obtained. It has been established that various types of economic activity lead to specific changes in the antibiotic resistance, which characterizes the soil of a natural grass-grass meadow (back-ground). Isolates with resistance to nalidixic acid, amoxicillin and ceftriaxone were found in the sample taken on the territory of the chemical plant more often than in the soil of the background site. The proportion of strains resistant to nalidixic acid, lincomycin and azithromycin was significantly (P<0.05) higher in the soil samples taken at the MSW collection site and the territory of the medical institution, while those resistant to nalidixic acid and amoxicillin were in the sample from the plywood factory Groups of antibiotics (quinolones – nalidixic acid, and β-lactams – amoxicillin and ceftriaxone) were identified, the resistance to which in streptomyces isolates from soils involved in economic activity was significantly higher than in soil isolates from the background territory. The data obtained in the work indicate the need to monitor the spread of antibiotic resistance in soils that are not only at risk of accumulation of residual concentrations of antibiotics, but also other consequences of anthropogenic influences.

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Field-based evidence for the enrichment of intrinsic antibiotic resistome stimulated by plant-derived fertilizer in agricultural soil

Cited by 5 publications

References 65 publications

What role do biocontrol agents with Mg ²⁺ play in the fate of antibiotic resistome and pathogenic bacteria in the phyllosphere?

What role do biocontrol agents with Mg ²⁺ play in the fate of antibiotic resistome and pathogenic bacteria in the phyllosphere?

Fecal antibiotic resistance genes were transferred through the distribution of soil-lettuce-snail food chain

Spread of antibiotic-resistant actinobacteria in soils exposed to various types of anthropogenic impact

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Field-based evidence for the enrichment of intrinsic antibiotic resistome stimulated by plant-derived fertilizer in agricultural soil

Cited by 5 publications

References 65 publications

What role do biocontrol agents with Mg 2+ play in the fate of antibiotic resistome and pathogenic bacteria in the phyllosphere?

What role do biocontrol agents with Mg 2+ play in the fate of antibiotic resistome and pathogenic bacteria in the phyllosphere?

Fecal antibiotic resistance genes were transferred through the distribution of soil-lettuce-snail food chain

Spread of antibiotic-resistant actinobacteria in soils exposed to various types of anthropogenic impact

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What role do biocontrol agents with Mg ²⁺ play in the fate of antibiotic resistome and pathogenic bacteria in the phyllosphere?

What role do biocontrol agents with Mg ²⁺ play in the fate of antibiotic resistome and pathogenic bacteria in the phyllosphere?