Effects of straw burning on pathogens and antibiotic resistance genes in paddy fields with bacterial leaf blight

doi:10.3785/j.issn.1008-9209.2023.01.131

Journal of Zhejiang University (Agriculture and Life Sciences)

2023, Vol. 49

Issue (6): 840-852 DOI: 10.3785/j.issn.1008-9209.2023.01.131

Resource utilization & environmental protection

Effects of straw burning on pathogens and antibiotic resistance genes in paddy fields with bacterial leaf blight

Binhao WANG^1,²(

),Yanbo CHEN^1,²,Rongjie LIU³,Dongqun WANG⁴,Zuozhen DONG⁵,Rui DI⁶,Xiao WANG⁷,Yuping WU⁸(

)

^1.College of Environmental and Resource Sciences, Zhejiang University, Hangzhou 310058, Zhejiang, China
^2.Hangzhou Global Scientific and Technological Innovation Center, Zhejiang University, Hangzhou 311200, Zhejiang, China
^3.Ninghai Agricultural Technology Extension Station, Ningbo 315600, Zhejiang, China
^4.Cixi Agricultural Monitoring Center, Ningbo 315300, Zhejiang, China
^5.Agricultural Technology Management and Service Station of Haishu District in Ningbo, Ningbo 315012, Zhejiang, China
^6.Agricultural Technology Extension Station of Zhenhai District in Ningbo, Ningbo 315200, Zhejiang, China
^7.Agricultural Technology Extension Service Station of Jiangbei District in Ningbo, Ningbo 315033, Zhejiang, China
^8.Ningbo Agricultural and Rural Green Development Center, Ningbo 315012, Zhejiang, China

Download:

HTML

HTML ( )

PDF(3212KB)
Export: BibTeX | EndNote (RIS)

Abstract

Bacterial leaf blight in rice is a significant disease, and understanding the effects of straw burning on pathogens and antibiotic resistance genes (ARGs) in paddy fields is crucial. Soil and rice stubble samples were collected from bacterial leaf blight outbreak areas in Ningbo City of Zhejiang Province, and these samples were subjected to high-throughput metagenomic sequencing to investigate the effects of straw burning. The results indicated that the relative abundance of pathogens in the rice stubble was significantly higher than that in the soil. After straw burning, except for the significant increase in available potassium content, there were no significant changes in the other physicochemical properties of the soil. Overall, there were no significant differences in pathogen community diversity after straw burning, but straw burning led to a sharp decrease in the relative abundance of Xanthomonas oryzae in the rice stubble. The relative abundances of ARGs in the soil and rice stubble increased after straw burning, but there were no significant differences compared with those before straw burning (P＞0.05), while the relative abundance of mobile genetic elements (MGEs) in the rice stubble decreased significantly after straw burning (P＜0.05). The proportion of positively correlated links in the coexisting networks of pathogens-ARGs decreased after straw burning. Mantel analysis revealed that the water content (r=0.642, p＜0.01), pH value (r=0.582, p＜0.05), total organic carbon content (r=0.325, p＜0.05), total nitrogen content (r=0.570, p＜0.01), and available phosphorus content (r=0.311, p＜0.05) were closely related to the soil ARG subtypes; the dissolved organic carbon (DOC) content (r=0.275, p＜0.05) and available potassium content (r=0.312, p＜0.05) were correlated with the ARG subtypes, and the DOC content (r=0.201, p＜0.05) significantly affected the pathogen community structure in the rice stubble. In summary, straw burning can reduce the relative abundance of X. oryzae in the rice stubble, which suggests that it may be a viable option for preventing and controlling rice bacterial leaf blight; moreover, a reduction in the positive correlation ratio of pathogens-ARGs and in the relative abundance of MGEs after straw burning may inhibit the formation of potentially resistant pathogens. However, given the complexity of soil biological compound pollution, the effects of straw burning on pathogens and ARGs in paddy fields need to be further explored by long-term location experiments.

Key words： straw burning bacterial leaf blight pathogens antibiotic resistance genes

Received: 13 January 2023 Published: 25 December 2023

CLC:

S182

Corresponding Authors: Yuping WU E-mail: wangbh7@zju.edu.cn;a_angelfish@163.com

	Service
	E-mail this article
	Add to my bookshelf
	Add to citation manager
	E-mail Alert
	RSS
	Articles by authors
	Binhao WANG
	Yanbo CHEN
	Rongjie LIU
	Dongqun WANG
	Zuozhen DONG
	Rui DI
	Xiao WANG
	Yuping WU

Cite this article:

Binhao WANG,Yanbo CHEN,Rongjie LIU,Dongqun WANG,Zuozhen DONG,Rui DI,Xiao WANG,Yuping WU. Effects of straw burning on pathogens and antibiotic resistance genes in paddy fields with bacterial leaf blight. Journal of Zhejiang University (Agriculture and Life Sciences), 2023, 49(6): 840-852.

URL:

https://www.zjujournals.com/agr/10.3785/j.issn.1008-9209.2023.01.131 OR https://www.zjujournals.com/agr/Y2023/V49/I6/840

秸秆焚烧对白叶枯病稻田中致病菌和抗生素抗性基因的影响

白叶枯病是水稻的重要病害之一。为了解秸秆焚烧对稻田土壤中病原菌和抗生素抗性基因（antibiotic resistance genes, ARGs）的影响，从浙江省宁波市水稻白叶枯病暴发区分别采集土壤和稻茬样品，并对采集的样品进行宏基因组高通量测序。结果表明：稻茬内致病菌相对丰度显著高于土壤，秸秆焚烧后土壤中除了速效钾含量显著升高，其他理化特性变化不明显。秸秆焚烧前后致病菌群落多样性总体上差异不明显，但是秸秆焚烧导致稻茬内水稻黄单胞菌（Xanthomonas oryzae）的相对丰度急剧降低。秸秆焚烧后土壤和稻茬内ARGs相对丰度提高，但与秸秆焚烧前差异不显著（P＞0.05），而稻茬内移动基因元件（mobile genetic elements, MGEs）相对丰度显著降低（P＜0.05）。此外，秸秆焚烧后致病菌和ARGs共存网络中正相关连接数占比有所下降。曼特尔（Mantel）分析表明：含水量（r=0.642，p＜0.01）、pH值（r=0.582，p＜0.05）、总有机碳含量（r=0.325，p＜0.05）、总氮含量（r=0.570，p＜0.01）和有效磷含量（r=0.311，p＜0.05）与土壤ARGs组成密切相关；而溶解有机碳含量（r=0.275，p＜0.05）和速效钾含量（r=0.312，p＜0.05）与稻茬内ARGs组成相关，且溶解有机碳含量（r=0.201，p＜0.05）显著影响稻茬内致病菌群落结构。综上所述，秸秆焚烧降低了稻茬内水稻黄单胞菌的相对丰度，暗示可以通过秸秆焚烧防控水稻白叶枯病；同时，致病菌和ARGs正相关共存关系的减弱和MGEs相对丰度的降低也表明秸秆焚烧可能遏制潜在耐药致病菌的形成。鉴于对土壤生物复合污染影响的复杂性，秸秆焚烧对稻田致病菌和抗生素抗性基因的影响还需要长期定位试验来进一步探讨。

关键词： 秸秆焚烧, 白叶枯病, 致病菌, 抗生素抗性基因

Table 1 Study area and sample collection

Fig. 1 Changes in soil physicochemical properties before and after straw burningDifferent lowercase letters above bars indicate significant differences at the 0.05 probability level. The same as below.

Fig. 2 Proportions of pathogen abundances and the relative abundances of major pathogen genera in the soil (A, B) and the rice stubble (C, D) before and after straw burning

Fig. 3 Changes in relative abundances of Xanthomonas and X.oryzae before and after straw burningA. Genus level; B. Species level.

Fig. 4 Differences of pathogen community compositions before and after straw burningA, C. α-diversity; B, D. β-diversity.

Fig. 5 Profiles of antibiotic resistance genes (ARGs), changes in relative abundances of ARGs and mobile genetic elements (MGEs) in the soil (A-C) and the rice stubble (D-F) before and after straw burning

Fig. 6 Correlation analysis on the relative abundances of ARGs and MGEs with the relative abundances of pathogens before and after straw burning

Fig. 7 Coexistence analysis of pathogens-ARGs and correlation analysis between co-occurrence network topology features and environmental factors in the soil (A-C) and the rice stubble (D-F) before and after straw burningSingle asterisk (*) indicates significant correlations at the 0.05 probability level.

Fig. 8 Correlation analysis of pathogen community structures (A) and ARG subtypes (B) in the soil and rice stubble with the soil physicochemical factorsThe color of the line represents the statistical significance of Mantel test, and the width of the line corresponds to Mantel test statistics; the correlation between environmental factors is displayed through a color gradient.


[1]	严东权,薛颖昊,徐志宇,等.我国农作物秸秆直接还田利用现状、技术模式及发展建议[J].中国农业资源与区划,2023,44(4):1-14. DOI:10.7621/cjarrp.1005-9121.20230401 YAN D Q, XUE Y H, XU Z Y, et al. Current utilization status, technical models and development proposals for direct crop straw returning to field in China[J]. Chinese Journal of Agricultural Resources and Regional Planning, 2023, 44(4): 1-14. (in Chinese with English abstract) doi: 10.7621/cjarrp.1005-9121.20230401

[2]	薛颖昊,冯浩杰,孙仁华,等.农作物秸秆肥料化利用研究文献计量分析[J].中国农业资源与区划,2023,44(1):108-118. DOI:10.7621/cjarrp.1005-9121.20230111 XUE Y H, FENG H J, SUN R H, et al. Bibliometric analysis of crop straw fertilizer utilization[J]. Chinese Journal of Agricultural Resources and Regional Planning, 2023, 44(1): 108-118. (in Chinese with English abstract) doi: 10.7621/cjarrp.1005-9121.20230111

[3]	陈利锋,徐敬友.农业植物病理学:南方本[M].北京:中国农业出版社,2001. CHEN L F, XU J Y. Agricultural Plant Pathology: Southern Edition[M]. Beijing: China Agriculture Press, 2001. (in Chinese)

[4]	翟婧,吴水祥,赵丽稳,等.宁波市水稻白叶枯病重发原因分析与防控对策思考[J].中国植保导刊,2022,42(8):85-88. DOI:10.3969/j.issn.1672-6820.2022.08.022 ZHAI J, WU S X, ZHAO L W, et al. Analysis on causes of rice white leaf blight and countermeasures in Ningbo City[J]. China Plant Protection, 2022, 42(8): 85-88. (in Chinese) doi: 10.3969/j.issn.1672-6820.2022.08.022

[5]	XIONG W, ZHAO Q Y, XUE C, et al. Comparison of fungal community in black pepper-vanilla and vanilla monoculture systems associated with vanilla Fusarium wilt disease[J]. Frontiers in Microbiology, 2016, 7: 117. DOI: 10.3389/fmicb.2016.00117 doi: 10.3389/fmicb.2016.00117

[6]	WEI Z, YU D. Rhizosphere fungal community structure succession of Xinjiang continuously cropped cotton[J]. Fungal Biology, 2019, 123(1): 42-50. DOI: 10.1016/j.funbio.2018.11.007 doi: 10.1016/j.funbio.2018.11.007

[7]	XIONG W, ZHAO Q Y, ZHAO J, et al. Different continuous cropping spans significantly affect microbial community membership and structure in a vanilla-grown soil as revealed by deep pyrosequencing[J]. Microbial Ecology, 2015, 70(1): 209-218. DOI: 10.1007/s00248-014-0516-0 doi: 10.1007/s00248-014-0516-0

[8]	LU L H, YIN S X, LIU X, et al. Fungal networks in yield-invigorating and -debilitating soils induced by prolonged potato monoculture[J]. Soil Biology and Biochemistry, 2013, 65: 186-194. DOI: 10.1016/j.soilbio.2013.05.025 doi: 10.1016/j.soilbio.2013.05.025

[9]	李明,吴发启,蒋碧,等.小麦秸秆焚烧对土壤有机质及微生物和玉米产量的影响[J].干旱地区农业研究,2013,31(2):95-99. DOI:10.3969/j.issn.1000-7601.2013.02.018 LI M, WU F Q, JIANG B, et al. Effects of crops straw burning on soil organic matter, soil microbes and mean grain yield[J]. Agricultural Research in the Arid Areas, 2013, 31(2): 95-99. (in Chinese with English abstract) doi: 10.3969/j.issn.1000-7601.2013.02.018

[10]	田国成,孙路,施明新,等.小麦秸秆焚烧对土壤有机质积累和微生物活性的影响[J].植物营养与肥料学报,2015,21(4):1081-1087. DOI:10.11674/zwyf.2015.0429 TIAN G C, SUN L, SHI M X, et al. Effect of wheat straw burning on soil organic matter accumulation and microbial activity[J]. Journal of Plant Nutrition and Fertilizers, 2015, 21(4): 1081-1087. (in Chinese with English abstract) doi: 10.11674/zwyf.2015.0429

[11]	张雄.原子吸收分光光度计测定土壤速效钾[J].南方农业,2018,12(35):112,114. DOI:10.19415/j.cnki.1673-890x.2018.35.058 ZHANG X. Determination of available potassium in soils by atomic absorption spectrophotometer[J]. South China Agriculture, 2018, 12(35): 112, 114. (in Chinese) doi: 10.19415/j.cnki.1673-890x.2018.35.058

[12]	鲍士旦.土壤农化分析[M].3版.北京:中国农业出版社,2000. BAO S D. Soil Agrochemical Analysis[M]. 3rd ed. Beijing: China Agriculture Press, 2000. (in Chinese)

[13]	BOLGER A M, LOHSE M, USADEL B. Trimmomatic: a flexible trimmer for Illumina sequence data[J]. Bioinformatics, 2014, 30(15): 2114-2120. DOI: 10.1093/bioinformatics/btu170 doi: 10.1093/bioinformatics/btu170

[14]	OUNIT R, WANAMAKER S, CLOSE T J, et al. CLARK: fast and accurate classification of metagenomic and genomic sequences using discriminative k-mers[J]. BMC Genomics, 2015, 16: 236. DOI: 10.1186/s12864-015-1419-2 doi: 10.1186/s12864-015-1419-2

[15]	YIN X L, JIANG X T, CHAI B L, et al. ARGs-OAP v2.0 with an expanded SARG database and hidden Markov models for enhancement characterization and quantification of antibiotic resistance genes in environmental metagenomes[J]. Bioinformatics, 2018, 34(13): 2263-2270. DOI: 10.1093/bioinformatics/bty053 doi: 10.1093/bioinformatics/bty053

[16]	PÄRNÄNEN K, KARKMAN A, HULTMAN J, et al. Maternal gut and breast milk microbiota affect infant gut antibiotic resistome and mobile genetic elements[J]. Nature Communications, 2018, 9: 3891. DOI: 10.1038/s41467-018-06393-w doi: 10.1038/s41467-018-06393-w

[17]	BURGESS L W, BACKHOUSE D, SWAN L J, et al. Control of Fusarium crown rot of wheat by late stubble burning and rotation with sorghum[J]. Australasian Plant Pathology, 1996, 25(4): 229-233. DOI: 10.1071/AP96042 doi: 10.1071/AP96042

[18]	OTERO-JIMÉNEZ V, DEL PILAR CARREÑO-CARREÑO J, BARRETO-HERNANDEZ E, et al. Impact of rice straw management strategies on rice rhizosphere microbiomes[J]. Applied Soil Ecology, 2021, 167: 104036. DOI: 10.1016/j.apsoil.2021.104036 doi: 10.1016/j.apsoil.2021.104036

[19]	ZHU H, WANG Z X, LUO X M, et al. Effects of straw incorporation on Rhizoctonia solani inoculum in paddy soil and rice sheath blight severity[J]. The Journal of Agricultural Science, 2014, 152(5): 741-748. DOI: 10.1017/S002185961300035X doi: 10.1017/S002185961300035X

[20]	LANOISELET V M, COTTIER E J, ASH G J, et al. Prevalence and survival, with emphasis on stubble burning, of Rhizoctonia spp., causal agents of sheath diseases of rice in Australia[J]. Australasian Plant Pathology, 2005, 34(2): 135-142. DOI: 10.1071/AP05010 doi: 10.1071/AP05010

[21]	CHOI O, KIM H, LEE Y, et al. First report of sheath rot of rice caused by Pantoea ananatis in Korea[J]. The Plant Pathology Journal, 2012, 28(3): 331. DOI: 10.5423/PPJ.DR.08.2011.0150 doi: 10.5423/PPJ.DR.08.2011.0150

[22]	MANOHARAN G, LALITHA P, JEGANATHAN L P, et al. Pantoea ananatis as a cause of corneal infiltrate after rice husk injury[J]. Journal of Clinical Microbiology, 2012, 50(6): 2163-2164. DOI: 10.1128/JCM.06743-11 doi: 10.1128/JCM.06743-11

[23]	魏华炜.秸秆基质协同污泥好氧堆肥及资源化利用中抗生素抗性基因风险研究[D].上海:华东师范大学,2020. WEI H W. Study on the risk of antibiotic resistance genes in straw substrate synergistic sludge compositing and resource utilization[D]. Shanghai: East China Normal University, 2020. (in Chinese with English abstract)

[24]	李洪林,刘凤艳,龚振平,等.稻秆还田对水稻主要病害发生的影响[J].作物研究,2012,26(1):7-10. DOI:10.3969/j.issn.1001-5280.2012.01.03 LI H L, LIU F Y, GONG Z P, et al. Effect of straw return back to paddy field on occurrence of rice major diseases[J]. Crop Research, 2012, 26(1): 7-10. (in Chinese with English abstract) doi: 10.3969/j.issn.1001-5280.2012.01.03

[25]	乔玉强,曹承富,赵竹,等.秸秆还田与施氮量对小麦产量和品质及赤霉病发生的影响[J].麦类作物学报,2013,33(4):727-731. DOI:10.7606/j.issn.1009-1041.2013.04.18 QIAO Y Q, CAO C F, ZHAO Z, et al. Effects of straw-returning and N-fertilizer application on yield, quality and occurrence of Fusarium head blight of wheat[J]. Journal of Triticeae Crops, 2013, 33(4): 727-731. (in Chinese with English abstract) doi: 10.7606/j.issn.1009-1041.2013.04.18

[26]	CHEN Z Y, ZHANG W, WANG G, et al. Bioavailability of soil-sorbed tetracycline to Escherichia coli under unsaturated conditions[J]. Environmental Science & Technology, 2017, 51(11): 6165-6173. DOI: 10.1021/acs.est.7b00590 doi: 10.1021/acs.est.7b00590

[27]	WU N, QIAO M, ZHANG B, et al. Abundance and diversity of tetracycline resistance genes in soils adjacent to repre-sentative swine feedlots in China[J]. Environmental Science & Technology, 2010, 44(18): 6933-6939. DOI: 10.1021/es1007802 doi: 10.1021/es1007802

[28]	XIAO K Q, LI B, MA L P, et al. Metagenomic profiles of antibiotic resistance genes (ARGs) in paddy soils from South China[J]. FEMS Microbiology Ecology, 2016, 92(3): fiw023. DOI: 10.1093/femsec/fiw023 doi: 10.1093/femsec/fiw023

[29]	生弘杰,王芳,相雷雷,等.土壤中抗生素抗性基因的环境行为与阻控研究进展[J].土壤学报,2023,60(1):39-49. DOI:10.11766/trxb202111100608 SHENG H J, WANG F, XIANG L L, et al. Environmental behavior and control of antibiotic resistance genes in soil: a review[J]. Acta Pedologica Sinica, 2023, 60(1): 39-49. (in Chinese with English abstract) doi: 10.11766/trxb202111100608

[1]	Jiannan ZHANG,Yiming WANG,Jiejing ZHANG,Lei CHEN,Jinyan LUO,Jianping YI,Bin LI,Qianli AN. *Detection and identification of Xanthomonas oryzae* pv. oryzicola using quantitative real-time PCR and digital PCR**[J]. Journal of Zhejiang University (Agriculture and Life Sciences), 2023, 49(1): 55-64.

[2]	ZHANG Yusen, YE Jun, SU Jianqiang. Antibiotic resistance in agroecosystem: Progress and challenges[J]. Journal of Zhejiang University (Agriculture and Life Sciences), 2017, 43(6): 691-699.

[3]	LU Haiyan, XU Chongxin, ZHANG Xiao, LIANG Ying, LIU Xianjin. Antibacterial effect of limonene on food-borne pathogens[J]. Journal of Zhejiang University (Agriculture and Life Sciences), 2016, 42(3): 306-312.

Viewed

Full text

Abstract

Cited

Shared

Discussed