The effect of long-term application of nitrogen-rich fertilizers on soil resistome: A study of conventional and organic cropping systems

Alexey S. Vasilchenko, Evgenii O. Burlakov, Darya V. Poshvina, Denis S. Gruzdev, Sergey V. Kravchenko, Aleksandr V. Iashnikov, Ning Ling, Anastasia V. Vasilchenko

PDF(5802 KB)
PDF(5802 KB)
Soil Ecology Letters ›› 2024, Vol. 6 ›› Issue (3) : 230215. DOI: 10.1007/s42832-023-0215-1
RESEARCH ARTICLE

The effect of long-term application of nitrogen-rich fertilizers on soil resistome: A study of conventional and organic cropping systems

Author information +
History +

Highlights

● Soil resistomes of conventional and organic systems were similar in terms of ARG biodiversity.

● Soil resistomes of conventional and organic systems were different regarding individual ARGs.

● Uncultivated bacteria and archaea can contribute significantly to soil resistome.

Abstract

Metagenomic studies of various soil environments have previously revealed the widespread distribution of antibiotic resistance genes (ARGs) around the globe. In this study, we applied shotgun metagenomics to investigate differences in microbial communities and resistomes in Chernozem soils that have been under long-term organic and conventional cropping practices. The organic cropping system was seeded with Triticum spelta without any fertilizer. The conventional cropping system was seeded with Tríticum durum Desf and used mineral fertilizer (NPK), that resulted in an increased amount of total and available carbon and nitrogen in soils. Across all samples, we identified a total of 21 ARG classes, among which the dominant were vancomycin, tetracycline and multidrug. Profiling of soil microbial communities revealed differences between the studied fields in the relative abundances of 14 and 53 genera in topsoil and subsoil, respectively. Correlation analysis showed significant correlations (positive and negative) among 18 genera and 6 ARGs, as well as between these ARGs and some chemical properties of soils. The analysis of metagenome-assembled genomes revealed that Nitrospirota, Thermoproteota, Actinobacteriota and Binatota phyla of archaea and bacteria serve as hosts for glycopeptide and fluoroquinolone/tetracycline ARGs. Collectively, the data obtained enrich knowledge about the consequences of human agricultural activities in terms of soil microbiome modification and highlight the role of nitrogen cycling taxa, including uncultivated genera, in the formation of soil resistome.

Graphical abstract

Keywords

soil microbiome / inorganic fertilizer / nitrogen cycle / uncultured bacteria / chemolithotrophs / Binatia

Cite this article

Download citation ▾
Alexey S. Vasilchenko, Evgenii O. Burlakov, Darya V. Poshvina, Denis S. Gruzdev, Sergey V. Kravchenko, Aleksandr V. Iashnikov, Ning Ling, Anastasia V. Vasilchenko. The effect of long-term application of nitrogen-rich fertilizers on soil resistome: A study of conventional and organic cropping systems. Soil Ecology Letters, 2024, 6(3): 230215 https://doi.org/10.1007/s42832-023-0215-1

References

[1]
Alcock, B.P., Huynh, W., Chalil, R., Smith, K.W., Raphenya, A.R., Wlodarski, M.A., Edalatmand, A., Petkau, A., Syed, S.A., Tsang, K.K., Baker, S.J.C., Dave, M., McCarthy, M.C., Mukiri, K.M., Nasir, J.A., Golbon, B., Imtiaz, H., Jiang, X., Kaur, K., Kwong, M., Liang, Z.C., Niu, K.C., Shan, P., Yang, J.Y.J., Gray, K.L., Hoad, G.R., Jia, B., Bhando, T., Carfrae, L.A., Farha, M.A., French, S., Gordzevich, R., Rachwalski, K., Tu, M.M., Bordeleau, E., Dooley, D., Griffiths, E., Zubyk, H.L., Brown, E.D., Maguire, F., Beiko, R.G., Hsiao, W.W.L., Brinkman, F.S.L., Van Domselaar, G., McArthur, A.G., 2023. CARD 2023: Expanded curation, support for machine learning, and resistome prediction at the comprehensive antibiotic resistance database. Nucleic Acids Research51, D690–D699.
CrossRef Google scholar
[2]
Alexopoulos, E.C., 2010. Introduction to multivariate regression analysis. Hippokratia14, 23–28.
[3]
Allen, H.K., Moe, L.A., Rodbumrer, J., Gaarder, A., Handelsman, J., 2009. Functional metagenomics reveals diverse beta-lactamases in a remote Alaskan soil. ISME Journal3, 243–251.
CrossRef Google scholar
[4]
Armalyte˙, J., Skerniškyte˙, J., Bakiene˙, E., Krasauskas, R., Šiugždiniene˙, R., Kareiviene˙, V., Kerziene˙, S., Klimiene˙, I., Sužiedėlienė, E., Ružauskas, M., Sužiedeliene˙ E., Ružauskas M., 2019. Microbial diversity and antimicrobial resistance profile in microbiota from soils of conventional and organic farming systems. Frontiers in Microbiology10, 892.
CrossRef Google scholar
[5]
Bill, M., Chidamba, L., Gokul, J.K., Labuschagne, N., Korsten, L., 2021. Bacterial community dynamics and functional profiling of soils from conventional and organic cropping systems. Applied Soil Ecology157, 103734.
CrossRef Google scholar
[6]
Blin, K., Shaw, S., Kloosterman, A.M., Charlop-Powers, Z., van Weezel, G.P., Medema, M.H., Weber, T., 2021. antiSMASH 6.0: improving cluster detection and comparison capabilities. Nucleic Acids Research 49, W29–W35.
[7]
Bolger, A.M., Lohse, M., Usadel, B., 2014. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics (Oxford, England)30, 2114–2120.
CrossRef Google scholar
[8]
Bowers, R.M., Kyrpides, N.C., Stepanauskas, R., Harmon-Smith, M., Doud, D., Reddy, T.B.K., Schulz, F., Jarett, J., Rivers, A.R., Eloe-Fadrosh, E.A., Tringe, S.G., Ivanova, N.N., Copeland, A., Clum, A., Becraft, E.D., Malmstrom, R.R., Birren, B., Podar, M., Bork, P., Weinstock, G.M., Garrity, G.M., Dodsworth, J.A., Yooseph, S., Sutton, G., Glöckner, F.O., Gilbert, J.A., Nelson, W.C., Hallam, S.J., Jungbluth, S.P., Ettema, T.J.G., Tighe, S., Konstantinidis, K.T., Liu, W.T., Baker, B.J., Rattei, T., Eisen, J.A., Hedlund, B., McMahon, K.D., Fierer, N., Knight, R., Finn, R., Cochrane, G., Karsch-Mizrachi, I., Tyson, G.W., Rinke, C., Lapidus, A., Meyer, F., Yilmaz, P., Parks, D.H., Murat Eren, A., Schriml, L., Banfield, J.F., Hugenholtz, P., Woyke, T., the Genome Standards Consortium, Lapidus, A., Meyer, F., Yilmaz, P., Parks, D.H., Eren, A.M., Schriml, L., Banfield, J.F., Hugenholtz, P., Woyke T., 2017. Minimum information about a single amplified genome (MISAG) and a metagenome-assembled genome (MIMAG) of bacteria and archaea. Nature Biotechnology35, 725–731.
CrossRef Google scholar
[9]
Brescia, F., Vlassi, A., Bejarano, A., Seidl, B., Marchetti-Deschmann, M., Schuhmacher, R., Puopolo, G., 2021. Characterisation of the antibiotic profile of Lysobacter capsici AZ78, an effective biological control agent of plant pathogenic microorganisms. Microorganisms17, 1320.
CrossRef Google scholar
[10]
Cadena, M., Durso, L.M., Miller, D.N., Waldrip, H.M., Castleberry, B.L., Drijber, R.A., Wortmann, C., 2018. Tetracycline and sulfonamide antibiotic resistance genes in soils from nebraska organic farming operations. Frontiers in Microbiology9, 1283.
CrossRef Google scholar
[11]
Chaumeil, P.A., Mussig, A.J., Hugenholtz, P., Parks, D.H., 2019. GTDB-Tk: a toolkit to classify genomes with the genome taxonomy database. Bioinformatics (Oxford, England)36, 1925–1927.
CrossRef Google scholar
[12]
Chen, Q., An, X., Li, H., Su, J., Ma, Y., Zhu, Y.G., 2016. Long-term field application of sewage sludge increases the abundance of antibiotic resistance genes in soil. Environment International 92–93, 1–10.
[13]
Chen, Y., Liu, X., Hou, Y., Zhou, S., Zhu, B., 2021. Particulate organic carbon is more vulnerable to nitrogen addition than mineral-associated organic carbon in soil of an alpine meadow. Plant and Soil458, 93–103.
CrossRef Google scholar
[14]
Chuvochina, M., Rinke, C., Parks, D.H., Rappé, M.S., Tyson, G.W., Yilmaz, P., Whitman, W.B., Hugenholtz, P., 2019. The importance of designating type material for uncultured taxa. Systematic and Applied Microbiology42, 15–21.
CrossRef Google scholar
[15]
Crémet, L., Bemer, P., Zambon, O., Reynaud, A., Caroff, N., Corvec, S., 2009. Chitinophaga terrae bacteremia in human. Emerging Infectious Diseases15, 1134–1135.
CrossRef Google scholar
[16]
D’Costa, V.M., McGrann, K.M., Hughes, D.W., Wright, G.D., 2006. Sampling the antibiotic resistome. Science311, 374–377.
CrossRef Google scholar
[17]
Delgado-Baquerizo, M., Hu, H.W., Maestre, F.T., Guerra, C.A., Eisenhauer, N., Eldridge, D.J., Zhu, Y.G., Chen, Q.L., Trivedi, P., Du, S., Makhalanyane, T.P., Verma, J.P., Gozalo, B., Ochoa, V., Asensio, S., Wang, L., Zaady, E., Illán, J.G., Siebe, C., Grebenc, T., Zhou, X., Liu, Y.R., Bamigboye, A.R., Blanco-Pastor, J.L., Duran, J., Rodríguez, A., Mamet, S., Alfaro, F., Abades, S., Teixido, A.L., Peñaloza-Bojacá, G.F., Molina-Montenegro, M.A., Torres-Díaz, C., Perez, C., Gallardo, A., García-Velázquez, L., Hayes, P.E., Neuhauser, S., He, J.Z., 2022. The global distribution and environmental drivers of the soil antibiotic resistome. Microbiome10, 219.
CrossRef Google scholar
[18]
Dinca, L.C., Grenni, P., Onet, C., Onet, A., 2022. Fertilization and soil microbial community: A review. Applied Sciences (Basel, Switzerland)12, 1198.
CrossRef Google scholar
[19]
Durner, W., Iden, S.C., von Unold, G., 2017. The integral suspension pressure method (ISP) for precise particle−size analysis by gravitational sedimentation. Water Resources Research53, 33–48.
CrossRef Google scholar
[20]
Edmeades, D.C., 2003. The long-term effects of manures and fertilisers on soil productivity and quality: a review. Nutrient Cycling in Agroecosystems66, 165–180.
CrossRef Google scholar
[21]
Epelde, L., Jauregi, L., Urra, J., Ibarretxe, L., Romo, J., Goikoetxea, I., Garbisu, C., 2018. Characterization of composted organic amendments for agricultural use. Frontiers in Sustainable Food Systems2, 44.
CrossRef Google scholar
[22]
Fosberg, K.J., Patel, S., Gibson, M.K., Lauber, C.L., Knight, R., Fierer, N., Dantas, G., 2016. Bacterial phylogeny structures soil resistomes across habitats. Nature5909, 612–616.
CrossRef Google scholar
[23]
Finn, R.D., Coggill, P., Eberhardt, R.Y., Eddy, S.R., Mistry, J., Mitchell, A.L., Potter, S.C., Punta, M., Qureshi, M., Sangrador-Vegas, A., Salazar, G.A., Tate, J., Bateman, A., 2016. The Pfam protein families database: towards a more sustainable future. Nucleic Acids Research44, D279–D285.
CrossRef Google scholar
[24]
Francioli, D., Schulz, E., Lentendu, G., Wubet, T., Buscot, F., Reitz, T., 2016. Mineral vs. organic amendments: Microbial community structure, activity and abundance of agriculturally relevant microbes are driven by long-term fertilization strategies. Frontiers in Microbiology7, 1446.
CrossRef Google scholar
[25]
Galperin, M.Y., Makarova, K.S., Wolf, Y.I., and Koonin, E.V., 2014. Expanded microbial genome coverage and improved protein family annotation in the COG database. Nucleic Acids Research43, D261–D269.
CrossRef Google scholar
[26]
Ghosh, S., Wilson, B., Ghoshal, S., Senapati, N., Mandal, B., 2012. Organic amendments influence soil quality and carbon sequestration in the Indo-Gangetic plains of India. Agriculture, Ecosystems & Environment156, 134–141.
CrossRef Google scholar
[27]
Gurevich, A., Saveliev, V., Vyahhi, N., Tesler, G., 2013. QUAST: quality assessment tool for genome assemblies. Bioinformatics (Oxford, England)29, 1072–1075.
CrossRef Google scholar
[28]
Hammer, Ø., Harper, D.A.T., Ryan, P.D., 2001. PAST: Paleontological statistics software package for education and data analysis. Palaeontologia Electronica,4, 9.
[29]
Hao, J., Chai, Y.N., Lopes, L.D., Ordóñez, R.A., Wright, E.E., Archontoulis, S., Schachtman, D.P., 2021. The effects of soil depth on the structure of microbial communities in agricultural soils in Iowa, USA. Applied and Environmental Microbiology87, e02673–e20.
CrossRef Google scholar
[30]
Iwata, K., Azlan, A., Yamakawa, H., Omori, T., 2010. Ammonia accumulation in culture broth by the novel nitrogen-fixing bacterium, Lysobacter sp. E4. Journal of Bioscience and Bioengineering 110, 415–418.
[31]
Ji, G.H., Wei, L.F., He, Y.Q., Wu, Y.P., Bai, X.H., 2008. Biological control of rice bacterial blight by Lysobacter antibioticus strain 13–1. Biological Control45, 288–296.
CrossRef Google scholar
[32]
Jochum, C., Osborne, L., Yuen, G., 2006. Fusarium head blight biological control with Lysobacter enzymogenes strain C3. Biological Control39, 336–344.
CrossRef Google scholar
[33]
Kang, D.D., Li, F., Kirton, E., Thomas, A., Egan, R., An, H., Wang, Z., 2019. MetaBAT 2: an adaptive binning algorithm for robust and efficient genome reconstruction from metagenome assemblies. PeerJ7, e7359.
CrossRef Google scholar
[34]
Kang, J., Liu, Y., Chen, X., Xu, F., Xiong, W., Li, X., 2022. Shifts of antibiotic resistomes in soil following amendments of antibiotics-contained dairy manure. International Journal of Environmental Research and Public Health19, 10804.
CrossRef Google scholar
[35]
Kaviani Rad, A., Astaykina, A., Streletskii, R., Afsharyzad, Y., Etesami, H., Zarei, M., Balasundram, S.K., 2022. An Overview of antibiotic resistance and abiotic stresses affecting antimicrobial resistance in agricultural soils. International Journal of Environmental Research and Public Health19, 4666.
CrossRef Google scholar
[36]
Kaze, M., Brooks, L., Sistrom, M., 2021. Antimicrobial resistance in Bacillus-based biopesticide products. Microbiology (Reading, England) 167.
[37]
Lawther, K., Santos, F.G., Oyama, L.B., Rubino, F., Morrison, S., Creevey, C.J., McGrath, J.W., Huws, S.A., 2022. Resistome analysis of global livestock and soil microbiomes. Frontiers in Microbiology13, 897905.
CrossRef Google scholar
[38]
Li, B., Yang, Y., Ma, L., Ju, F., Guo, F., Tiedje, J.M., Zhang, T., 2015. Metagenomic and network analysis reveal wide distribution and co-occurrence of environmental antibiotic resistance genes. ISME Journal9, 2490–2502.
CrossRef Google scholar
[39]
Li, H., 2018. Minimap2: pairwise alignment for nucleotide sequences. Bioinformatics (Oxford, England)34, 3094–3100.
CrossRef Google scholar
[40]
Li, S., Yao, Q., Liu, J., Wei, D., Zhou, B., Zhu, P., Cui, X., Jin, J., Liu, X., Wang, G., 2020. Profiles of antibiotic resistome with animal manure application in black soils of northeast China. Journal of Hazardous Materials384, 121216.
CrossRef Google scholar
[41]
Li, Y., Kong, F., Li, S., Wang, J., Hu, J., Chen, S., Chen, Q., Li, Y., Ha, X., Sun, W., 2023. Insights into the driving factors of vertical distribution of antibiotic resistance genes in long-term fertilized soils. Journal of Hazardous Materials456, 131706.
CrossRef Google scholar
[42]
Liu, P., Jia, S., He, X., Zhang, X., Ye, L., 2017. Different impacts of manure and chemical fertilizers on bacterial community structure and antibiotic resistance genes in arable soils. Chemosphere188, 455–464.
CrossRef Google scholar
[43]
Liu, W., Cheng, Y., Guo, J., Duan, Y., Wang, S., Xu, Q., Liu, M., Xue, C., Guo, S., Shen, Q., Ling, N., 2022. Long-term manure inputs induce a deep selection on agroecosystem soil antibiotic resistome. Journal of Hazardous Materials436, 129163.
CrossRef Google scholar
[44]
Liu, Z., Zhao, Y., Zhang, B., Wang, J., Zhu, L., Hu, B., 2023. Deterministic effect of pH on shaping soil resistome revealed by metagenomic analysis. Environmental Science & Technology57, 985–996.
CrossRef Google scholar
[45]
Miller, E.S., Woese, C.R., Brenner, S., 1991. Description of the erythromycin-producing bacterium Arthrobacter sp. strain NRRL B-3381 as Aeromicrobium erythreum gen. nov., sp. nov. International Journal of Systematic Bacteriology 41, 363–368
[46]
Murphy, C.L., Sheremet, A., Dunfield, P.F., Spear, J.R., Stepanauskas, R., Woyke, T., Elshahed, M.S., Youssef, N.H., 2021. Genomic analysis of the yet-uncultured Binatota reveals broad methylotrophic, alkane-degradation, and pigment production capacities. mBio12, e00985–e21.
CrossRef Google scholar
[47]
Nesme, J., Simonet, P., 2015. The soil resistome: a critical review on antibiotic resistance origins, ecology and dissemination potential in telluric bacteria. Environmental Microbiology17, 913–930.
CrossRef Google scholar
[48]
Nissen, J.N., Johansen, J., Allesøe, R.L., Sønderby, C.K., Armenteros, J.J.A., Grønbech, C.H., Jensen, L.J., Nielsen, H.B., Petersen, T.N., Winther, O., Rasmussen, S., 2021. Improved metagenome binning and assembly using deep variational autoencoders. Nature Biotechnology39, 555–560.
CrossRef Google scholar
[49]
Nõlvak, M.T., Kanger, K., Tampere, M., Espenberg, M., Loit, E., Raave, H., Truu, J., 2016. Inorganic and organic fertilizers impact the abundance and proportion of antibiotic resistance and integron-integrase genes in agricultural grassland soil. Science of the Total Environment562, 678–689.
CrossRef Google scholar
[50]
Nurk, S., Meleshko, D., Korobeynikov, A., Pevzner, P.A., 2017. metaSPAdes: a new versatile metagenomic assembler. Genome Research27, 824–834.
CrossRef Google scholar
[51]
Okonechnikov, K., Conesa, A., García-Alcalde, F., 2016. Qualimap 2: advanced multi-sample quality control for high-throughput sequencing data. Bioinformatics (Oxford, England)32, 292–294.
CrossRef Google scholar
[52]
Pansu, M., Gautheyrou, J., 2007. Handbook of Soil Analysis: Mineralogical, Organic and Inorganic Methods. Springer Berlin, Heidelberg
[53]
Parks, D.H., Imelfort, M., Skennerton, C.T., Hugenholtz, P., Tyson, G.W., 2015. CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes. Genome Research25, 1043–1055.
CrossRef Google scholar
[54]
Pathak, P., Reddy, A.S., 2021. Vertical distribution analysis of soil organic carbon and total nitrogen in different land use patterns of an agro-organic farm. Tropical Ecology62, 386–397.
CrossRef Google scholar
[55]
Puopolo, G., Raio, A., Zoina, A., 2010. Identification and characterization of Lysobacter capsici strain PG4: A new plant health-promoting rhizobacterium. Journal of Plant Pathology92, 157–164.
CrossRef Google scholar
[56]
Qian, X., Gunturu, S., Guo, J., Chai, B., Cole, J.R., Gu, J., Tiedje, J.M., 2021. Metagenomic analysis reveals the shared and distinct features of the soil resistome across tundra, temperate prairie, and tropical ecosystems. Microbiome9, 108.
CrossRef Google scholar
[57]
Qiu, D., Ke, M., Zhang, Q., Zhang, F., Lu, T., Sun, L., Qian, H., 2022. Response of microbial antibiotic resistance to pesticides: An emerging health threat. Science of the Total Environment850, 158057.
CrossRef Google scholar
[58]
Rodríguez-Ramos, J.A., Borton, M.A., McGivern, B.B., Smith, G.J., Solden, L.M., Shaffer, M., Daly, R.A., Purvine, S.O., Nicora, C.D., Eder, E.K., Lipton, M., Hoyt, D.W., Stegen, J.C., Wrighton, K.C., 2022. Genome-resolved metaproteomics decodes the microbial and viral contributions to coupled carbon and nitrogen cycling in river sediments. mSystems7, e0051622.
CrossRef Google scholar
[59]
Rchiad, Z., Dai, M., Hamel, C., Bainard, L.D., Cade-Menun, B.J., Terrat, Y., St-Arnaud, M., Hijri, M., 2022. Soil depth significantly shifted microbial community structures and functions in a semiarid prairie agroecosystem. Frontiers in Microbiology13, 815890.
CrossRef Google scholar
[60]
Rubinfeld, D.L., 2011. Reference Guide on Multiple Regression, in Reference Manual on Scientific Evidence: Third Edition. National Academies Press, Wahington, DC
[61]
Ruppé, E., Ghozlane, A., Tap, J., Pons, N., Alvarez, A.S., Maziers, N., Cuesta, T., Hernando-Amado, S., Clares, I., Martínez, J.L., Coque, T.M., Baquero, F., Lanza, V.F., Máiz, L., Goulenok, T., de Lastours, V., Amor, N., Fantin, B., Wieder, I., Andremont, A., van Schaik, W., Rogers, M., Zhang, X., Willems, R.J.L., de Brevern, A.G., Batto, J.M., Blottière, H.M., Léonard, P., Léjard, V., Letur, A., Levenez, F., Weiszer, K., Haimet, F., Doré, J., Kennedy, S.P., Ehrlich, S.D., 2019. Prediction of the intestinal resistome by a three-dimensional structure-based method. Nature Microbiology4, 112–123.
CrossRef Google scholar
[62]
Sanz, C., Casadoi, M., Tadic, Đ., Pastor-López, E.J., Navarro-Martin, L., Parera, J., Tugues, J., Ortiz, C.A., Bayona, J.M., Piña, B., 2022. Impact of organic soil amendments in antibiotic levels, antibiotic resistance gene loads, and microbiome composition in corn fields and crops. Environmental Research 214, 113760.
[63]
Seemann, T., 2014. Prokka: rapid prokaryotic genome annotation. Bioinformatics (Oxford, England)30, 2068–2069.
CrossRef Google scholar
[64]
Sieber, C.M., Probst, A.J., Sharrar, A., Thomas, B.C., Hess, M., Tringe, S.G., Banfield, J.F., 2018. Recovery of genomes from metagenomes via a dereplication, aggregation and scoring strategy. Nature Microbiology3, 836–843.
CrossRef Google scholar
[65]
Sun, R., Guo, X., Wang, D., Chu, H., 2015. Effects of long-term application of chemical and organic fertilizers on the abundance of microbial communities involved in the nitrogen cycle. Applied Soil Ecology95, 171–178.
CrossRef Google scholar
[66]
Van Goethem, M.W., Pierneef, R., Bezuidt, O.K.I., Van De Peer, Y., Cowan, D.A., Makhalanyane, T.P., 2018. A reservoir of ‘historical’ antibiotic resistance genes in remote pristine Antarctic soils. Microbiome6, 40.
CrossRef Google scholar
[67]
Vance, E.D., Brookes, P.C., Jenkinson, D.S., 1987. An extraction method for measuring soil microbial biomass C. Soil Biology & Biochemistry19, 703–707.
CrossRef Google scholar
[68]
Venturini, A.M., Gontijo, J.B., Mandro, J.A., Paula, F.S., Yoshiura, C.A., da França, A.G., Tsai, S.M., 2022. Genome-resolved metagenomics reveals novel archaeal and bacterial genomes from Amazonian forest and pasture soils. Microbial Genomics8, mgen000853.
CrossRef Google scholar
[69]
Wang, F., Han, W., Chen, S., Dong, W., Qiao, M., Hu, C., Liu, B., 2020A. Fifteen-year application of manure and chemical fertilizers differently impacts soil ARGs and microbial community structure. Frontiers in Microbiology 11, 62
[70]
Wang, J., Tu, X., Zhang, H., Cui, J., Ni, K., Chen, J., Cheng, Y., Zhang, J., Chang, S.X., 2020B. Effects of ammonium-based nitrogen addition on soil nitrification and nitrogen gas emissions depend on fertilizer-induced changes in pH in a tea plantation soil. Science of the Total Environment 747, 141340
[71]
Wu, Y.W., Simmons, B.A., Singer, S.W., 2016. MaxBin 2.0: an automated binning algorithm to recover genomes from multiple metagenomic datasets. Bioinformatics (Oxford, England) 32, 605–607.
[72]
Yin, X.L., Jiang, X.T., Chai, B.L., Li, L.G., Yang, Y., Cole, J.R., Tiedje, J.M., Zhang, T., 2018. 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. Bioinformatics 34, 2263–2270
[73]
Xie, W.Y., Yuan, S.T., Xu, M.G., Yang, X.P., Shen, Q.R., Zhang, W.W., Su, J.Q., Zhao, F.J., 2018. Long-term effects of manure and chemical fertilizers on soil antibiotic resistome. Soil Biology & Biochemistry122, 111–119.
CrossRef Google scholar
[74]
Xu, Y., Li, H., Tan, L., Li, Q., Liu, W., Zhang, C., Gao, Y., Wei, X., Gong, Q., Zheng, X., 2016. Alterations in soil microbial community composition and biomass following agricultural land use change. Scientific Reports6, 36587.
CrossRef Google scholar
[75]
Yang, Y., Jiang, X.T., Chai, B.L., Ma, L.P., Li, B., Zhang, A.N., Cole, J.R., Tiedje, J.M., Zhang, T., 2016. ARGs-OAP: online analysis pipeline for antibiotic resistance genes detection from metagenomic data using an integrated structured ARG-database. Bioinform.32, 2346–2351.
CrossRef Google scholar
[76]
Zhang, Q., Wu, J., Yang, F., Lei, Y., Zhang, Q., Cheng, X., 2016. Alterations in soil microbial community composition and biomass following agricultural land use change. Scientific Reports6, 36587.
CrossRef Google scholar

Funding

This study was supported by the Ministry of Science and Higher Education of the Russian Federation within the framework of the Federal Scientific and Technical Program for the Development of Genetic Technologies for 2019-2027 (agreement Nº075-15-2021-1345, unique identifier RF— -193021X0012).

Conflicts of interest

The authors declare no conflict of interest.

Author contributions

Conceptualization, A.S.V.; methodology, A.S.V., E.O.B., A.V.V.; formal analysis, A.S.V., E.O.B., A.V.V.; investigation, D.S.G., D.V.P., S.V.K., A.V.I.; resources, A.S.V.; data curation, A.S.V., A.V.V.; writing—original draft preparation, A.S.V.; writing—review and editing, N.L.; funding acquisition, A.S.V. All authors have read and agreed to the published version of the manuscript.

Acknowledgments

We acknowledged Dr. Natalya Tomashevich (Federal Scientific Center for Biological Plant Protection, Krasnodar, Russia) for her assistance in selecting study sites. This work was partially performed using resources of the Research Resource Center & Natural Resource Management and Physico-Chemical Research (University of Tyumen).

RIGHTS & PERMISSIONS

2023 Higher Education Press
AI Summary AI Mindmap
PDF(5802 KB)

Accesses

Citations

Detail

Sections
Recommended

/