The occurrence of banana Fusarium wilt aggravates antibiotic resistance genes dissemination in soil

Jiabao Wang; Yannan Ou; Ruochen Li; Chengyuan Tao; Hongjun Liu; Rong Li; Zongzhuan Shen; Qirong Shen

Ecotoxicology and Environmental Safety (Sep 2024)

The occurrence of banana Fusarium wilt aggravates antibiotic resistance genes dissemination in soil

Jiabao Wang,
Yannan Ou,
Ruochen Li,
Chengyuan Tao,
Hongjun Liu,
Rong Li,
Zongzhuan Shen,
Qirong Shen

Affiliations

Jiabao Wang: The Sanya Institute of the Nanjing Agricultural University, Key Lab of Organic-Based Fertilizers of China, Jiangsu Provincial Key Lab for Solid Organic Waste Utilization, Jiangsu Collaborative Innovation Center of Solid Organic Wastes, Educational Ministry Engineering Center of Resource-Saving Fertilizers, Nanjing Agricultural University, Nanjing, Jiangsu 210095, China
Yannan Ou: The Sanya Institute of the Nanjing Agricultural University, Key Lab of Organic-Based Fertilizers of China, Jiangsu Provincial Key Lab for Solid Organic Waste Utilization, Jiangsu Collaborative Innovation Center of Solid Organic Wastes, Educational Ministry Engineering Center of Resource-Saving Fertilizers, Nanjing Agricultural University, Nanjing, Jiangsu 210095, China
Ruochen Li: The Sanya Institute of the Nanjing Agricultural University, Key Lab of Organic-Based Fertilizers of China, Jiangsu Provincial Key Lab for Solid Organic Waste Utilization, Jiangsu Collaborative Innovation Center of Solid Organic Wastes, Educational Ministry Engineering Center of Resource-Saving Fertilizers, Nanjing Agricultural University, Nanjing, Jiangsu 210095, China
Chengyuan Tao: The Sanya Institute of the Nanjing Agricultural University, Key Lab of Organic-Based Fertilizers of China, Jiangsu Provincial Key Lab for Solid Organic Waste Utilization, Jiangsu Collaborative Innovation Center of Solid Organic Wastes, Educational Ministry Engineering Center of Resource-Saving Fertilizers, Nanjing Agricultural University, Nanjing, Jiangsu 210095, China
Hongjun Liu: The Sanya Institute of the Nanjing Agricultural University, Key Lab of Organic-Based Fertilizers of China, Jiangsu Provincial Key Lab for Solid Organic Waste Utilization, Jiangsu Collaborative Innovation Center of Solid Organic Wastes, Educational Ministry Engineering Center of Resource-Saving Fertilizers, Nanjing Agricultural University, Nanjing, Jiangsu 210095, China
Rong Li: The Sanya Institute of the Nanjing Agricultural University, Key Lab of Organic-Based Fertilizers of China, Jiangsu Provincial Key Lab for Solid Organic Waste Utilization, Jiangsu Collaborative Innovation Center of Solid Organic Wastes, Educational Ministry Engineering Center of Resource-Saving Fertilizers, Nanjing Agricultural University, Nanjing, Jiangsu 210095, China
Zongzhuan Shen: Corresponding author at: College of Resources and Environmental Sciences, Nanjing Agricultural University, Nanjing 210095, China.; The Sanya Institute of the Nanjing Agricultural University, Key Lab of Organic-Based Fertilizers of China, Jiangsu Provincial Key Lab for Solid Organic Waste Utilization, Jiangsu Collaborative Innovation Center of Solid Organic Wastes, Educational Ministry Engineering Center of Resource-Saving Fertilizers, Nanjing Agricultural University, Nanjing, Jiangsu 210095, China
Qirong Shen: The Sanya Institute of the Nanjing Agricultural University, Key Lab of Organic-Based Fertilizers of China, Jiangsu Provincial Key Lab for Solid Organic Waste Utilization, Jiangsu Collaborative Innovation Center of Solid Organic Wastes, Educational Ministry Engineering Center of Resource-Saving Fertilizers, Nanjing Agricultural University, Nanjing, Jiangsu 210095, China

Journal volume & issue: Vol. 283
p. 116982

Abstract

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The spread of antibiotic resistance genes (ARGs) and subsequent soil-borne disease outbreaks are major threats to soil health and sustainable crop production. However, the relationship between occurrences of soil-borne diseases and the transmission of soil ARGs remains unclear. Here, soil ARGs, mobile genetic elements and microbial communities from co-located disease suppressive and conducive banana orchards were deciphered using metagenomics and metatranscriptomics approaches. In total, 23 ARG types, with 399 subtypes, were detected using a metagenomics approach, whereas 23 ARG types, with 452 subtypes, were discovered using a metatranscriptomics method. Furthermore, the metagenomics analysis revealed that the ARG total abundance levels were greater in rhizospheres (0.45 ARGs/16S rRNA on average) compared with bulk (0.32 ARGs/16S rRNA on average) soils. Interestingly, metatranscriptomics revealed that the total ARG abundances were greater in disease-conducive (8.85 ARGs/16S rRNA on average) soils than disease suppressive (1.45 ARGs/16S rRNA on average) soils. Mobile genetic elements showed the same trends as ARGs. Network and binning analyses indicated that Mycobacterium, Streptomyces, and Blastomonas are the main potential hosts of ARGs. Furthermore, Bacillus was significantly and negatively correlated with Fusarium (P < 0.05, r = −0.84) and hosts of ARGs (i.e., Mycobacterium, Streptomyces, and Blastomonas). By comparing metagenomic and metatranscriptomic analyses，this study demonstrated that metatranscriptomics may be more sensitive in indicating ARGs activities in soil. Our findings enable the more accurate assessment of the transmission risk of ARGs. The data provide a new perspective for recognizing soil health, in which soil-borne disease outbreaks appear to be associated with ARG spread, whereas beneficial microbe enrichment may mitigate wilt disease and ARG transmission.

Published in Ecotoxicology and Environmental Safety

ISSN: 0147-6513 (Print); 1090-2414 (Online)
Publisher: Elsevier
Country of publisher: United States
LCC subjects: Technology: Environmental technology. Sanitary engineering: Environmental pollution; Geography. Anthropology. Recreation: Environmental sciences
Website: https://www.journals.elsevier.com/ecotoxicology-and-environmental-safety

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