强还原处理对土壤中常见抗生素及其抗性基因的影响研究

doi:10.16258/j.cnki.1674-5906.2024.07.012

生态环境学报 ›› 2024, Vol. 33 ›› Issue (7): 1107-1116.DOI: 10.16258/j.cnki.1674-5906.2024.07.012

• 研究论文【环境科学】 • 上一篇下一篇

强还原处理对土壤中常见抗生素及其抗性基因的影响研究

林于蓝¹(), 陈厚朴¹, 于文豪¹, 王宝英¹^,², 张杨², 张金波¹^,³^,⁴, 蔡祖聪¹^,³^,⁴, 赵军¹^,³^,⁴^,^*()

1.南京师范大学地理科学学院，江苏南京 210023
2.南京师范大学生命科学学院，江苏南京 210023
3.江苏省土壤利用与农业可持续发展工程研究中心，江苏南京 210023
4.江苏省地理信息资源开发和利用协同创新中心，江苏南京 210023

收稿日期:2024-03-26 出版日期:2024-07-18 发布日期:2024-09-04
通讯作者: *赵军。E-mail: junzhao37@njnu.edu.cn
作者简介:林于蓝（1999年生），女，硕士研究生，主要研究方向为土壤微生物与抗生素污染修复。E-mail: yllin613@163.com
基金资助:
国家自然科学基金项目(42090065);国家自然科学基金项目(42307385);江苏省农业农村污染防治技术与装备工程研究中心开放资金项目(GCZXZD2301);江苏省研究生科研与实践创新计划项目(KYCX22_1568);江苏省研究生科研与实践创新计划项目(KYCX23_1720);南京师范大学学生科学基金项目(NSTW2022056)

Effects of Reductive Soil Disinfestation on Common Antibiotics and Their Antibiotic Resistance Genes in Soil

LIN Yulan¹(), CHEN Houpu¹, YU Wenhao¹, WANG Baoying¹^,², ZHANG Yang², ZHANG Jinbo¹^,³^,⁴, CAI Zucong¹^,³^,⁴, ZHAO Jun¹^,³^,⁴^,^*()

1. School of Geography, Nanjing Normal University, Nanjing 210023, P. R. China
2. School of Life Sciences, Nanjing Normal University, Nanjing 210023, P. R. China
3. Jiangsu Engineering Research Center for Soil Utilization & Sustainable Agriculture, Nanjing 210023, P. R. China
4. Jiangsu Center for Collaborative Innovation in Geographical Information Resource Development and Application, Nanjing 210023, P. R. China

Received:2024-03-26 Online:2024-07-18 Published:2024-09-04

摘要/Abstract

摘要：

土壤中抗生素长期累积所引发的抗性致病菌富集以及抗性基因（Antibiotic resistance genes，ARGs）的传播扩散，已成为当前备受关注的环境问题。为研究强还原处理（Reductive soil disinfestation，RSD）对土壤中抗生素及其ARGs的影响，以常用且难降解的抗生素四环素、土霉素、磺胺嘧啶和磺胺甲恶唑所构建的质量分数为20 mg∙kg⁻¹的抗生素混合污染土壤为研究对象，分别设置以玉米秸秆（2%，RCS）、甘蔗渣（2%，RSR）为有机物料的RSD处理，同时设置不处理对照，于处理第7、14、28天进行破坏性采样，利用高效液相色谱和荧光定量PCR技术分析RSD处理过程中抗生素质量分数及ARGs和可移动遗传元件（Mobile genetic elements，MGEs）丰度的变化。结果表明，RSD处理可有效降解土壤中的四环素类和磺胺类抗生素，处理28 d后磺胺类抗生素的降解率为45.2%－100%，优于四环素类的33.5%－57.2%；RSR处理对四环素和磺胺嘧啶的降解效果优于RCS处理，其降解率可达57.2%－64.8%，而RCS处理对土霉素的降解率可达44.7%；两种RSD处理对磺胺甲恶唑的降解率在14 d时即可达100%。RSD处理后土壤中ARGs绝对丰度显著增加，RCS处理的增加作用强于RSR处理；随处理时间延长，tetM、qacH等基因相对丰度在RSD处理中呈下降趋势，一定程度上表明ARGs增加带来的生态负面效应得到缓解。RSD处理可显著降低IS26基因的相对丰度，表明其能通过消减特定MGEs削弱ARGs水平转移能力。综上，RSD处理可有效降解土壤中四环素类和磺胺类抗生素，具有消减土壤中ARGs并降低其传播风险的潜力。研究结果可为解决土壤抗生素污染问题、降低ARGs扩散风险提供一定的理论与技术支持。

关键词: 强还原土壤处理, 抗生素, 抗生素抗性基因, 可移动遗传元件, 降解效应

Abstract:

The enrichment of antibiotic-resistant pathogens and the spread of antibiotic resistance genes (ARGs) caused by the long-term accumulation of antibiotics in soil has become an environmental issue of great concern. To investigate the effect of reductive soil disinfestation (RSD) on antibiotics and associated ARGs, four antibiotics (tetracycline, oxytetracycline, sulfadiazine, and sulfamethoxazole) were selected, which are commonly used and are difficult to degrade, and a mixed antibiotic-contaminated soil was constructed. Each antibiotic was administered at a dose of 20 mg∙kg⁻¹. Three treatments, CK (control without soil treatment), RCS (RSD incorporated with 2% corn straw), and RSR (RSD incorporated with 2% sugarcane bagasse), were performed and destructive sampling was conducted on days 7, 14, and 28. High-performance liquid chromatography and fluorescence quantitative PCR were used to analyze the changes in antibiotic concentrations as well as the abundance of ARGs and mobile genetic elements (MGEs) during RSD treatment. The results showed that RSD treatment effectively degraded tetracyclines and sulfonamides in the soil. After 28 days of treatment, the degradation rate of sulfonamides was 45.2%-100%, which was better than that of tetracyclines, ranging from 33.5% to 57.2%. The RSR treatment had a better degradation effect on tetracycline and sulfadiazine than the RCS treatment, with degradation rates of up to 57.2%-64.8%, while the opposite was true for oxytetracycline, which was degraded up to 44.7% by the RCS treatment. The degradation of sulfamethoxazole by both RSD treatments was up to 100% after 14 days of treatment. The antibiotic concentration gradually decreased with the treatment time, and the two RSD treatments had different degradation effects on antibiotics. The absolute abundance of ARGs in the soil increased significantly after RSD treatment, and the effect of RCS treatment was stronger than that of the RSR treatment. With the extension of the treatment time, the relative abundance of ARGs such as tetM and qacH decreased in the RSD treatments, suggesting that the negative ecological effects of the increased ARGs were mitigated. The RSD treatment significantly reduced the relative abundance of IS26 in soil, suggesting that it can impair the horizontal transfer capacity of ARGs by ablating specific MGEs. Overall, RSD treatment can effectively degrade tetracyclines and sulfonamides in soil, and has the potential to reduce the abundance of ARGs and the risk of their spread. This study provides some theoretical and technical support for solving the problem of soil antibiotic contamination and reducing the risk of ARGs spread.

Key words: reductive soil disinfestation, antibiotics, antibiotic resistance genes, mobile genetic elements, degradation effects

中图分类号:

林于蓝, 陈厚朴, 于文豪, 王宝英, 张杨, 张金波, 蔡祖聪, 赵军. 强还原处理对土壤中常见抗生素及其抗性基因的影响研究[J]. 生态环境学报, 2024, 33(7): 1107-1116.

LIN Yulan, CHEN Houpu, YU Wenhao, WANG Baoying, ZHANG Yang, ZHANG Jinbo, CAI Zucong, ZHAO Jun. Effects of Reductive Soil Disinfestation on Common Antibiotics and Their Antibiotic Resistance Genes in Soil[J]. Ecology and Environment, 2024, 33(7): 1107-1116.

图/表 9

表1 定量PCR引物

Table 1 Primers used in PCR quantifications

基因类型		引物	序列 (5′-3′)
细菌	16S rRNA	Eub338F	ACTCCTACGGGAGGCAGCAG
细菌	16S rRNA	Eub518R	ATTACCGCGGCTGCTGG
磺胺类 ARGs	sul1	sul1-f	CACCGGAAACATCGCTGCA
磺胺类 ARGs	sul1	sul1-r	AAGTTCCGCCGCAAGGCT
四环素类 ARGs	tetM	tetM-f	GGAGCGATTACAGAATTAGGAAGC
	tetM	tetM-f	TCCATATGTCCTGGCGTGTC
	tetG	tetG-f	GCTCGGTGGTATCTCTGCTC
	tetG	tetG-r	AGCAACAGAATCGGGAACAC
多药类 ARGs	qacH	qacH-f	GTCGGTGTTGCTTATGCAGTCT
	qacH	qacH-r	CAACCAGGCAATGGCTGTAA
	msrE	msrE-f	CGGCAGATGGTCTGAGCTTAAA
	msrE	msrE-r	CGCACTCTTCCTGCATAAAGGA
可移动遗传元件 MGEs	IS26	IS26-f	ATGGATGAAACCTACGTGAAGGTC
	IS26	IS26-r	CGGTACTTAATCTGTCGGTGTTCA
	IS6100	IS6100-f	CGCACCGGCTTGATCAGTA
	IS6100	IS6100-f	CTGCCACGCTCAATACCGA
	intl1	intl1-f	GCCTTGATGTTACCCGAGAG
	intl1	intl1-r	GATCGGTCGAATGCGTGT

图1 不同处理中抗生素质量分数的变化图中数据为平均值±标准差（n=3）；不同大写字母表示同一处理方式不同处理时间内差异显著；不同小写字母表示同一处理时间不同处理方式内差异显著（p <0.05）。下同

Figure 1 Changes in antibiotic mass fraction in different treatments

表2 RSD处理相对于CK处理对抗生素的降解率

Table 2 Degradation rates of antibiotics by RSD treatment compared to CK treatment

抗生素类型	处理方式	抗生素降解率/%						多元方差分析
抗生素类型	处理方式	d7	p	d14	p	d28	p	处理时间	处理方式	处理时间×处理方式
四环素	RCS	−11.3±9.45	ns	3.15±5.03	ns	33.5±11.6	ns	***	ns	*
四环素	RSR	−7.03±5.98	ns	−2.11±1.73	ns	57.2±9.16	ns	***	ns	*
土霉素	RCS	−1.26±12.8	ns	17.0±11.5	ns	44.7±11.8	ns	***	ns	ns
土霉素	RSR	−14.4±7.64	ns	27.5±0.81	ns	39.9±7.65	ns	***	ns	ns
磺胺嘧啶	RCS	42.6±6.44	ns	2.95±8.47	ns	45.2±20.9	ns	**	ns	ns
磺胺嘧啶	RSR	43.2±5.94	ns	32.3±21.7	ns	64.8±3.40	ns	**	ns	ns
磺胺甲恶唑	RCS	88.3±5.64	ns	100±0	ns	100±0	ns	***	ns	ns
磺胺甲恶唑	RSR	91.6±1.43	ns	100±0	ns	100±0	ns	***	ns	ns

表3 不同处理中细菌数量的变化

Table 3 Changes in bacterial populations in different treatments

处理方式	细菌数量/(lg copies∙g⁻¹)
处理方式	d7	d14	d28
CK	9.51±0.03Ac	9.65±0.10Ac	9.62±0.12Ab
RCS	10.4±0.04Aa	10.5±0.04Aa	10.6±0.15Aa
RSR	10.3±0.05Ab	10.3±0.02Ab	10.5±0.01Aa

图2 不同处理中ARGs绝对丰度的变化

Figure 2 Changes in absolute abundances of ARGs in different treatments

图3 不同处理中ARGs相对丰度的变化

Figure 3 Changes in relative abundances of ARGs in different treatments

图4 不同处理中MGEs绝对和相对丰度的变化

Figure 4 Changes in absolute and relative abundances of MGEs in different treatments

图5 抗生素质量分数和细菌与ARGs和MGEs间的相关性红色和蓝色分别表示两变量间的正相关和负相关关系，颜色越深表示关系越紧密。*、**和***分别表示p<0.05、p<0.01和p<0.001。下同

Figure 5 Correlation between antibiotic mass fraction and bacteria with ARGs and MGEs

图6 ARGs和MGEs间的相关性

Figure 6 Correlation between ARGs and MGEs

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强还原处理对土壤中常见抗生素及其抗性基因的影响研究

Effects of Reductive Soil Disinfestation on Common Antibiotics and Their Antibiotic Resistance Genes in Soil

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