Tomato bacterial wilt disease outbreaks are accompanied by an increase in soil antibiotic resistance

Ruochen Li; Na Zhang; Xuhui Deng; Chengyuan Tao; Xin Pei; Yang Yue; Xu Xu; Jiabao Wang; Zongzhuan Shen; Qirong Shen; Rong Li

Environment International (Aug 2024)

Tomato bacterial wilt disease outbreaks are accompanied by an increase in soil antibiotic resistance

Ruochen Li,
Na Zhang,
Xuhui Deng,
Chengyuan Tao,
Xin Pei,
Yang Yue,
Xu Xu,
Jiabao Wang,
Zongzhuan Shen,
Qirong Shen,
Rong Li

Affiliations

Ruochen Li: The Sanya Institute of the Nanjing Agricultural University, Jiangsu Provincial Key Lab of Solid Organic Waste Utilization, Jiangsu Collaborative Innovation Center of Solid Organic Wastes, Educational Ministry Engineering Center of Resource-saving Fertilizers, Nanjing Agricultural University, Nanjing 210095, Jiangsu, PR China
Na Zhang: The Sanya Institute of the Nanjing Agricultural University, Jiangsu Provincial Key Lab of Solid Organic Waste Utilization, Jiangsu Collaborative Innovation Center of Solid Organic Wastes, Educational Ministry Engineering Center of Resource-saving Fertilizers, Nanjing Agricultural University, Nanjing 210095, Jiangsu, PR China
Xuhui Deng: The Sanya Institute of the Nanjing Agricultural University, Jiangsu Provincial Key Lab of Solid Organic Waste Utilization, Jiangsu Collaborative Innovation Center of Solid Organic Wastes, Educational Ministry Engineering Center of Resource-saving Fertilizers, Nanjing Agricultural University, Nanjing 210095, Jiangsu, PR China
Chengyuan Tao: The Sanya Institute of the Nanjing Agricultural University, Jiangsu Provincial Key Lab of Solid Organic Waste Utilization, Jiangsu Collaborative Innovation Center of Solid Organic Wastes, Educational Ministry Engineering Center of Resource-saving Fertilizers, Nanjing Agricultural University, Nanjing 210095, Jiangsu, PR China
Xin Pei: The Sanya Institute of the Nanjing Agricultural University, Jiangsu Provincial Key Lab of Solid Organic Waste Utilization, Jiangsu Collaborative Innovation Center of Solid Organic Wastes, Educational Ministry Engineering Center of Resource-saving Fertilizers, Nanjing Agricultural University, Nanjing 210095, Jiangsu, PR China
Yang Yue: The Sanya Institute of the Nanjing Agricultural University, Jiangsu Provincial Key Lab of Solid Organic Waste Utilization, Jiangsu Collaborative Innovation Center of Solid Organic Wastes, Educational Ministry Engineering Center of Resource-saving Fertilizers, Nanjing Agricultural University, Nanjing 210095, Jiangsu, PR China
Xu Xu: The Sanya Institute of the Nanjing Agricultural University, Jiangsu Provincial Key Lab of Solid Organic Waste Utilization, Jiangsu Collaborative Innovation Center of Solid Organic Wastes, Educational Ministry Engineering Center of Resource-saving Fertilizers, Nanjing Agricultural University, Nanjing 210095, Jiangsu, PR China
Jiabao Wang: The Sanya Institute of the Nanjing Agricultural University, Jiangsu Provincial Key Lab of Solid Organic Waste Utilization, Jiangsu Collaborative Innovation Center of Solid Organic Wastes, Educational Ministry Engineering Center of Resource-saving Fertilizers, Nanjing Agricultural University, Nanjing 210095, Jiangsu, PR China
Zongzhuan Shen: Corresponding authors at: College of Resources and Environmental Sciences, Nanjing Agricultural University, 210095 Nanjing, PR China.; The Sanya Institute of the Nanjing Agricultural University, Jiangsu Provincial Key Lab of Solid Organic Waste Utilization, Jiangsu Collaborative Innovation Center of Solid Organic Wastes, Educational Ministry Engineering Center of Resource-saving Fertilizers, Nanjing Agricultural University, Nanjing 210095, Jiangsu, PR China
Qirong Shen: The Sanya Institute of the Nanjing Agricultural University, Jiangsu Provincial Key Lab of Solid Organic Waste Utilization, Jiangsu Collaborative Innovation Center of Solid Organic Wastes, Educational Ministry Engineering Center of Resource-saving Fertilizers, Nanjing Agricultural University, Nanjing 210095, Jiangsu, PR China
Rong Li: Corresponding authors at: College of Resources and Environmental Sciences, Nanjing Agricultural University, 210095 Nanjing, PR China.; The Sanya Institute of the Nanjing Agricultural University, Jiangsu Provincial Key Lab of Solid Organic Waste Utilization, Jiangsu Collaborative Innovation Center of Solid Organic Wastes, Educational Ministry Engineering Center of Resource-saving Fertilizers, Nanjing Agricultural University, Nanjing 210095, Jiangsu, PR China

Journal volume & issue: Vol. 190
p. 108896

Abstract

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The presence of soil-borne disease obstacles and antibiotic resistance genes (ARGs) in soil leads to serious economic losses and health risks to humans. One area in need of attention is the evolution of ARGs as pathogenic soil gradually develops, which introduces uncertainty to the dynamic ability of conventional farming models to predict ARGs. Here, we investigated variations in tomato bacterial wilt disease accompanied by the resistome by metagenomic analysis in soils over 13 seasons of monoculture. The results showed that the abundance and diversity of ARGs and mobile genetic elements (MGEs) exhibited a significant and positive correlation with R. solanacearum. Furthermore, the binning approach indicated that fluoroquinolone (qepA), tetracycline (tetA), multidrug resistance genes (MDR, mdtA, acrB, mexB, mexE), and β-lactamases (ampC, blaGOB) carried by the pathogen itself were responsible for the increase in overall soil ARGs. The relationships between pathogens and related ARGs that might underlie the breakdown of soil ARGs were further studied in R. solanacearum invasion pot experiments. This study revealed the dynamics of soil ARGs as soil-borne diseases develop, indicating that these ecological trends can be anticipated. Overall, this study enhances our understanding of the factors driving ARGs in disease-causing soils.

Published in Environment International

ISSN: 0160-4120 (Print)
Publisher: Elsevier
Country of publisher: United Kingdom
LCC subjects: Geography. Anthropology. Recreation: Environmental sciences
Website: https://www.journals.elsevier.com/environment-international

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