Long-distance responses of ginger to soil sulfamethoxazole and chromium: Growth, co-occurrence with antibiotic resistance genes, and consumption risk

Jia-Min Xu; Yao Lv; Kun Xu; Xiaohui Liu; Kai Wang; Hu-Yi Zi; Guodong Zhang; Ai-Jie Wang; Shaoyong Lu; Hao-Yi Cheng

doi:10.1016/j.envpol.2023.122081

Long-distance responses of ginger to soil sulfamethoxazole and chromium: Growth, co-occurrence with antibiotic resistance genes, and consumption risk

Environ Pollut. 2023 Oct 1:334:122081. doi: 10.1016/j.envpol.2023.122081. Epub 2023 Jul 4.

Authors

Jia-Min Xu¹, Yao Lv², Kun Xu², Xiaohui Liu³, Kai Wang², Hu-Yi Zi¹, Guodong Zhang⁴, Ai-Jie Wang¹, Shaoyong Lu³, Hao-Yi Cheng⁵

Affiliations

¹ School of Civil and Environmental Engineering, Harbin Institute of Technology-Shenzhen (HIT-SZ), Shenzhen, 518055, China; State Key Laboratory of Urban Water Resources and Environment, School of Civil and Environmental Engineering, Harbin Institute of Technology Shenzhen, Shenzhen, 518055, China.
² College of Horticulture Science and Engineering, Shandong Agricultural University, Taian, 271018, China.
³ State Key Laboratory of Environmental Criteria and Risk Assessment, National Engineering Laboratory for Lake Pollution Control and Ecological Restoration, Chinese Research Academy of Environmental Sciences, Beijing, 100012, China.
⁴ College of Natural Resources and Environment, Northwest A&F University, Yangling, Shaanxi, 712100, China.
⁵ School of Civil and Environmental Engineering, Harbin Institute of Technology-Shenzhen (HIT-SZ), Shenzhen, 518055, China; State Key Laboratory of Urban Water Resources and Environment, School of Civil and Environmental Engineering, Harbin Institute of Technology Shenzhen, Shenzhen, 518055, China. Electronic address: chenghaoyi@hit.edu.cn.

PMID: 37414118
DOI: 10.1016/j.envpol.2023.122081

Abstract

The coexistence of antibiotics and heavy metals in agroecosystems is nonnegligible, which permits the promotion of antibiotic resistance genes (ARGs) in crops, thus posing a potential threat to humans along the food chain. In this study, we investigated the bottom-up (rhizosphere→rhizome→root→leaf) long-distance responses and bio-enrichment characteristics of ginger to different sulfamethoxazole (SMX) and chromium (Cr) contamination patterns. The results showed that ginger root systems adapted to SMX- and/or Cr-stress by increasing humic-like exudates, which may help to maintain the rhizosphere indigenous bacterial phyla (i.e., Proteobacteria, Chloroflexi, Acidobacteria and Actinobacteria). The root activity, leaf photosynthesis and fluorescence, and antioxidant enzymes (SOD, POD, CAT) of ginger were significantly decreased under high-dose Cr and SMX co-contamination, while a "hormesis effect" was observed under single low-dose SMX contamination. For example, CS100 (co-contamination of 100 mg/L SMX and 100 mg/L Cr) caused the most severe inhibition to leaf photosynthetic function by reducing photochemical efficiency (reflected on PAR-ETR, φPSII and qP). Meanwhile, CS100 induced the highest ROS production, in which H₂O₂ and O₂^·- increased by 328.82% and 238.00% compared with CK (the blank control without contamination). Moreover, co-selective stress by Cr and SMX induced the increase of ARG bacterial hosts and bacterial phenotypes containing mobile elements, contributing to the high detected abundance of target ARGs (sul1, sul2) up to 10^-2∼10^-1 copies/16S rRNA in rhizomes intended for consumption.

Keywords: Agriculture products security; Antibiotic resistance; Chromium; Ginger growth; Sulfamethoxazole.

MeSH terms

Anti-Bacterial Agents* / pharmacology
Bacteria / genetics
Chromium / toxicity
Drug Resistance, Microbial / genetics
Genes, Bacterial
Humans
Hydrogen Peroxide
RNA, Ribosomal, 16S
Soil
Sulfamethoxazole
Zingiber officinale* / genetics

Substances

Anti-Bacterial Agents
Sulfamethoxazole
ginger extract
Soil
Chromium
RNA, Ribosomal, 16S
Hydrogen Peroxide