Widespread use of antibiotics has led to an increase in the virulence factors (VFs) and antibiotic resistance genes (ARGs) within soil microbial communities. However, the impact of agricultural management, plant type and soil compartment on the distribution of VFs and ARGs in both organic systems and conventional systems remains unclear. In this study, we conducted a metagenomic analysis to investigate the distribution. Nonmetric multidimensional scaling analysis revealed that soil samples exhibited clustering primarily based on agricultural management system for both VFs (stressVFDB = 0.071) and ARGs (stressARDB = 0.117, stressCARD = 0.069). We observed significantly higher levels of VFs and ARGs in soils from conventional systems compared with organic systems (p < 0.05). Furthermore, combined analysis of carbohydrate-active enzymes (CAZymes) and KEGG revealed that six classes comprising 445 families of CAZymes were significantly more abundant in conventional system soils than in organic system soils. Notably, the abundance of carbamyl phosphate synthase (ammonia) was relatively higher in organic system samples (53.33%) compared with conventional system samples (48.8%). Our comprehensive analysis suggests that different agricultural management practices lead to alterations in soil microbial communities. Specifically, organic management practices were found to effectively mitigate the pathogenic potential and drug resistance of soil microbial communities. In conclusion, our findings highlight the substantial influence of agricultural management on soil microbial communities, with corresponding clustering patterns observed in VFs and ARGs. Organic farming practices contribute to the promotion of healthier soil microsystems and the sustainable development of agriculture compared with conventional systems.
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References
1.
AlbrightMBN, JohansenR, LopezD, et al.Short-Term transcriptional response of microbial communities to nitrogen fertilization in a pine forest soil Michaeline. Appl Environ Microbiol, 2018; 84(15); doi: 10.1128/aem.00598-18
2.
AndradeAC, FróesA, LopesFAC, et al.Diversity of microbial carbohydrate-active enZYmes (CAZYmes) associated with freshwater and soil samples from caatinga biome. Microb Ecol, 2017; 74(1):89–105; doi: 10.1007/s00248-016-0911-9
3.
AndréI, Potocki-VéronèseG, BarbeS, et al.CAZyme discovery and design for sweet dreams. Curr Opin Chem Biol, 2014; 19:17–24; doi: 10.1016/j.cbpa.2013.11.014
4.
BernardSM, HabashDZ. The importance of cytosolic glutamine synthetase in nitrogen assimilation and recycling. New Phytol, 2009; 182(3):608–620; doi: 10.1111/j.1469-8137.2009.02823.x
5.
BingZ, YuX, XianghuaW, et al.The composition and spatial patterns of bacterial virulence factors and antibiotic resistance genes in 19 wastewater treatment plants. PLoS One, 2016; 11(12):e0167422.
6.
CantarelBL, CoutinhoPM, RancurelC, et al.The carbohydrate-active EnZymes database (CAZy): An expert resource for Glycogenomics. Nucleic Acids Res, 2009; 37(Database issue):D233–D238; doi: 10.1093/nar/gkn663
7.
CaoRK, BenWW, QiangZM, et al.Removal of antibiotic resistance genes in pig manure composting influenced by inoculation of compound microbial agents. Bioresour Technol, 2020; 317:123966; doi: 10.1016/j.biortech.2020.123966
8.
CarkaciD, HojholtK, NielsenXC, et al.Genomic characterization, phylogenetic analysis, and identification of virulence factors in Aerococcus sanguinicola and Aerococcus urinae strains isolated from infection episodes. Microb Pathog, 2017; 112:327–340; doi: 10.1016/j.micpath.2017.09.042
9.
ChellapandiP, PrisillaA. Clostridium botulinum type A-virulome-gut interactions: A systems biology insight. Human Microbiome Journal, 2018; 7–8:15–22; doi: 10.1016/j.humic.2018.01.003
10.
ChenQ, AnX, LiH, et al.Long-term field application of sewage sludge increases the abundance of antibiotic resistance genes in soil. Environ Int, 2016a;92–93:1–10; doi: 10.1016/j.envint.2016.03.026
11.
ChenYR, GuoXP, NiuZS, et al.Antibiotic resistance genes (ARGs) and their associated environmental factors in the Yangtze Estuary, China: From inlet to outlet. Mar Pollut Bull, 2020; 158:111360; doi: 10.1016/j.marpolbul.2020.111360
12.
ChenJ, McIlroySE, ArchanaA, et al.A pollution gradient contributes to the taxonomic, functional, and resistome diversity of microbial communities in marine sediments. Microbiome, 2019; 7(1):104; doi: 10.1186/s40168-019-0714-6
13.
ChengDM, FengY, LiuY, et al.Dynamics of oxytetracycline, sulfamerazine, and ciprofloxacin and related antibiotic resistance genes during swine manure composting. J Environ Manage, 2019; 230:102–109; doi: 10.1016/j.jenvman.2018.09.074
14.
ChenB, YuanK, ChenX, et al.Metagenomic analysis revealing Antibiotic Resistance Genes (ARGs) and their genetic compartments in the Tibetan environment. Environ Sci Technol, 2016b;50(13):6670–6679.
15.
DoTT, NolanS, HayesN, et al.Metagenomic and HT-qPCR analysis reveal the microbiome and resistome in pig slurry under storage, composting, and anaerobic digestion. Environ Pollut, 2022; 305:119271; doi: 10.1016/j.envpol.2022.119271
16.
FahrenfeldN, KnowltonK, KrometisLA, et al.Effect of Manure Application on Abundance of Antibiotic Resistance Genes and Their Attenuation Rates in Soil: Field-Scale Mass Balance Approach. Environ Sci Technol, 2014; 48(5):2643–2650; doi: 10.1021/es404988k
17.
FengHW, SunYJ, ZhiY, et al.Identification and characterization of the nitrate assimilation genes in the isolate of Streptomyces griseorubens JSD-1. Microb Cell Fact, 2014; 13:174; doi: 10.1186/s12934-014-0174-4
18.
FresiaP, AnteloV, SalazarC, et al.Urban metagenomics uncover antibiotic resistance reservoirs in coastal beach and sewage waters. Microbiome, 2019; 7(1):35.
19.
GarbevaP, Van VeenJA, Van ElsasJD. Microbial diversity in soil: Selection microbial populations by plant and soil type and implications for disease suppressiveness. Annu Rev Phytopathol, 2004; 42:243–270; doi: 10.1146/annurev.phyto.42.012604.135455
20.
GillingsMR. Evolutionary consequences of antibiotic use for the resistome, mobilome and microbial pangenome. Front Microbiol, 2013; 4:4; doi: 10.3389/fmicb.2013.00004
21.
HashmiMZ, MahmoodA, KattelDB, et al.Antibiotics and Antibiotic Resistance Genes (ARGs) in soil: Occurrence, fate, and effects. In: Xenobiotics in the Soil Environment. Soil Biology. (HashmiM, KumarV, VarmaA eds.). Springer: Cham; 2017. p. 49.
22.
HeLY, YingGG, LiuYS, et al.Discharge of swine wastes risks water quality and food safety: Antibiotics and antibiotic resistance genes, from swine sources to the receiving environments. Environ Int, 2016; 92–93:210–219; doi: 10.1016/j.envint.2016.03.023
23.
HennessyJE, LatterMJ, FazelinejadS, et al.Hyperthermophilic carbamate kinase stability and anabolic In Vitro activity at alkaline pH. Appl Environ Microbiol, 2018; 84(3); doi: 10.1128/aem.02250-17
24.
HuaF, HuifangW, LinC, et al.Prevalence of antibiotic resistance genes and bacterial pathogens in long-term manured greenhouse soils as revealed by metagenomic survey. Environ Sci Technol, 2015; 49(2):1095–1104.
25.
JeongJ, SongWH, CooperWJ, et al.Degradation of tetracycline antibiotics: Mechanisms and kinetic studies for advanced oxidation/reduction processes. Chemosphere, 2010; 78(5):533–540; doi: 10.1016/j.chemosphere.2009.11.024
26.
KimJ, HuZP, CaiL, et al.CPS1 maintains pyrimidine pools and DNA synthesis in KRAS/LKB1-mutant lung cancer cells. Nature, 2017; 546(7656):168–172; doi: 10.1038/nature22359
27.
LeitaoJH. Microbial virulence factors. International Journal of Molecular Sciences, 2020; 21(15):5320.
28.
LiuBT, YuKF, AhmedI, et al.Key factors driving the fate of antibiotic resistance genes and controlling strategies during aerobic composting of animal manure: A review. Sci Total Environ, 2021; 791:148372; doi: 10.1016/j.scitotenv.2021.148372
29.
LuJQ, ZhangXX, WangCH, et al.Responses of sediment resistome, virulence factors and potential pathogens to decades of antibiotics pollution in a shrimp aquafarm. Sci Total Environ, 2021; 794:148760; doi: 10.1016/j.scitotenv.2021.148760
30.
MahapatraS, YadavR, RamakrishnaW. Bacillus subtilis impact on plant growth, soil health and environment: Dr. Jekyll and Mr. Hyde. J Appl Microbiol, 2022; 132(5):3543–3562; doi: 10.1111/jam.15480
31.
MarchiL, DegolaF, BaruffiniE, et al.How to easily detect plant NADH-glutamate dehydrogenase (GDH) activity? A simple and reliable in planta procedure suitable for tissues, extracts and heterologous microbial systems. Plant Sci, 2021; 304:110714; doi: 10.1016/j.plantsci.2020.110714
32.
McGivanJD, BradfordNM, Mendes-MourãoJ. The regulation of carbamoyl phosphate synthase activity in rat liver mitochondria. Biochem J, 1976; 154(2):415–421; doi: 10.1042/bj1540415
33.
PanY, ZengJ, LiL, et al.Coexistence of antibiotic resistance genes and virulence factors deciphered by large-scale complete genome analysis. mSystems, 2020; 5(3); doi: 10.1128/mSystems.00821-19
34.
PengS, FengY, WangY, et al.Prevalence of antibiotic resistance genes in soils after continually applied with different manure for 30 years. J Hazard Mater, 2017; 340:16–25; doi: 10.1016/j.jhazmat.2017.06.059
35.
PeyraudR, CottretL, MarmiesseL, et al.Control of primary metabolism by a virulence regulatory network promotes robustness in a plant pathogen. Nat Commun, 2018; 9(1):418; doi: 10.1038/s41467-017-02660-4
36.
QianX, SunW, GuJ, et al.Variable effects of oxytetracycline on antibiotic resistance gene abundance and the bacterial community during aerobic composting of cow manure. J Hazard Mater, 2016; 315:61–69; doi: 10.1016/j.jhazmat.2016.05.002
37.
SharmaR, LarneyFJ, ChenJ, et al.Selected antimicrobial resistance during composting of manure from cattle administered sub-therapeutic antimicrobials. J Environ Qual, 2009; 38(2):567–575; doi: 10.2134/jeq2007.0638
38.
ShennanC, KrupnikTJ, BairdG, et al.Organic and conventional agriculture: A useful framing? Annu Rev Environ Resour, 2017; 42(1):317–346.
39.
SinghJS, PandeyVC, SinghDP. Efficient soil microorganisms: a new dimension for sustainable agriculture and environmental development. Agriculture, Ecosystems & Environment, 2011; 140(3–4):339–353.
40.
SoborgDA, HendriksenNB, KilianM, et al.Widespread occurrence of bacterial human virulence determinants in soil and freshwater environments. Appl Environ Microbiol, 2013; 79(18):5488–5497; doi: 10.1128/aem.01633-13
41.
SuH, XuW, HuX, et al.Diversity and prevalence of antibiotic resistance genes, virulence factors, and the microbiome in Aquaculture in Southern China revealed by metagenomic sequencing. 2020.
42.
TangY, LiangZ, LiG, et al.Metagenomic profiles and health risks of pathogens and antibiotic resistance genes in various industrial wastewaters and the associated receiving surface water. Chemosphere, 2021; 283:131224; doi: 10.1016/j.chemosphere.2021.131224
43.
TranTT, ScottA, TienYC, et al.On-Farm anaerobic digestion of dairy manure reduces the abundance of antibiotic resistance-associated gene targets and the potential for plasmid transfer. Appl Environ Microbiol, 2021; 87(14):e0298020; doi: 10.1128/aem.02980-20
44.
VilcaFZ, PonceTEL, LoayzaODV, et al.Antibiotic ciprofloxacin in irrigation water: Its effect on medicago sativa (Alfalfa), including carbon fixation and root growth. Environmental Engineering Science, 2024; 41(7):271–277; doi: 10.1089/ees.2023.0329
45.
VincentL, HemalathaGR, ElodieD, et al.The carbohydrate-active enzymes database (CAZy) in 2013. Nucleic Acids Research, 2014; 42(Database issue):D490–D5.
46.
WangS, LiuC, WangX, et al.Dissimilatory nitrate reduction to ammonium (DNRA) in traditional municipal wastewater treatment plants in China: Widespread but low contribution. Water Res, 2020; 179:115877.
47.
WardmanJF, BainsRK, RahfeldP, et al.Carbohydrate-active enzymes (CAZymes) in the gut microbiome. Nat Rev Microbiol, 2022; 20(9):542–556; doi: 10.1038/s41579-022-00712-1
48.
XiaoE, SunW, DengJ, et al.The potential linkage between antibiotic resistance genes and microbial functions across soil–plant systems. Plant Soil, 2023; 493(1–2):589–602; doi: 10.1007/s11104-023-06247-5
49.
XieWY, YangXP, LiQ, et al.Changes in antibiotic concentrations and antibiotic resistome during commercial composting of animal manures. Environ Pollut, 2016; 219:182–190; doi: 10.1016/j.envpol.2016.10.044
50.
YangHY, DuanGC, ZhuJY, et al.Prevalence and characterisation of plasmid-mediated quinolone resistance and mutations in the gyrase and topoisomerase IV genes among Shigella isolates from Henan, China, between 2001 and 2008. Int J Antimicrob Agents, 2013; 42(2):173–177; doi: 10.1016/j.ijantimicag.2013.04.026
51.
YangY, JiangX, ChaiB, et al.ARGs-OAP: Online analysis pipeline for antibiotic resistance genes detection from metagenomic data using an integrated structured ARG-database. Bioinformatics, 2016; 32(15):2346–2351; doi: 10.1093/bioinformatics/btw136
52.
YangC, ZhaoYH, CaoW, et al.Metagenomic analysis reveals antibiotic resistance genes and virulence factors in the saline-alkali soils from the Yellow River Delta, China. Environ Res, 2022; 214(Pt 2):113823; doi: 10.1016/j.envres.2022.113823
53.
ZhangZ, WangY, ChenB, et al.Xenobiotic pollution affects transcription of antibiotic resistance and virulence factors in aquatic microcosms. Environ Pollut, 2022; 306:119396; doi: 10.1016/j.envpol.2022.119396
54.
ZhangS, YangG, HouS, et al.Distribution of ARGs and MGEs among glacial soil, permafrost, and sediment using metagenomic analysis. Environ Pollut, 2018; 234:339–346; doi: 10.1016/j.envpol.2017.11.031
55.
ZhouJ, FongJJ. Strong agricultural management effects on soil microbial community in a non-experimental agroecosystem. Applied Soil Ecology, 2021; 165:103970; doi: 10.1016/j.apsoil.2021.103970
56.
ZhuD, DingJ, WangY, et al.Effects of trophic level and land use on the variation of animal antibiotic resistome in the soil food web. Environ Sci Technol, 2022; 56(21):14937–14947.
57.
ZhuLJ, ZhaoY, YangKJ, et al.Host bacterial community of MGEs determines the risk of horizontal gene transfer during composting of different animal manures. Environ Pollut, 2019; 250:166–174; doi: 10.1016/j.envpol.2019.04.037
58.
ZouYA, XiaoZJ, WangLF, et al.Prevalence of antibiotic resistance genes and virulence factors in the sediment of WWTP effluent-dominated rivers. Sci Total Environ, 2023; 897:165441; doi: 10.1016/j.scitotenv.2023.165441
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