Distribution of antibiotic resistant bacteria in different soil types following manure application

Abstract

● ARB was investigated in different soil types following manure application.

● CTC-manure induced more resistance of soil indigenous microbes in fluvo-aquic soil.

● Lactobacillus , Dyella , Ralstonia , and Bacillus were the key different genera.

● Manure control is an effective way to reduce the risk of soil ARB.

Swine manure, commonly applied as organic compost in agricultural fields, is an important reservoir of antibiotic-resistant bacteria (ARB). Previous work indicated that manure application led to more antibiotic resistance genes in red soil compared with black soil and fluvo-aquic soil. Accordingly, the influencing mechanisms of soil types on the distribution of ARB was worthy of further exploration by a soil column experiment. The results showed that a higher shift in the operational taxonomic units and the community composition of chlortetracycline (CTC)-resistant bacteria (CRB) were observed in fluvo-aquic soil than in black and red soils. CTC induced antibiotic resistance development in soil indigenous microorganisms (Streptomyces, Pseudomonas, Bacillus, Rhodococcus, and Paenibacillus), and the induction was most obvious in fluvo-aquic soil. Streptomyces was significantly positively correlated with pH and organic matter. Additionally, LEfSe analysis indicated that the key different genera were Microbacteriaceae (black soil), Lactobacillus, unclassified_c__Bacilli and Paenibacillus (fluvo-aquic soil), and Dyella, Ralstonia and Bacillus (red soil). It was concluded that manure application led to higher CRB risk in fluvo-aquic soil compared with black and red soils. Overall, appropriate methods according to soil types are important ways to reduce the risk of soil resistant bacteria during manure return.

Graphical abstract

Keywords

chlortetracycline-resistant bacteria (CRB) / soil types / manure application / fluvo-aquic soil / LEfSe analysis

References

[1] Bengtsson-Palme, J., Kristiansson, E., Larsson, D.G.J., 2018. Environmental factors influencing the development and spread of antibiotic resistance. FEMS Microbiology Reviews42, 68–80.

[2] Boehme, S., Werner, G., Klare, I., Reissbrodt, R., Witte, W., 2004. Occurrence of antibiotic-resistant enterobacteria in agricultural foodstuffs. Molecular Nutrition & Food Research48, 522–531.

[3] Brandt, K.K., Amezquita, A.B., Thomas, B., Alistair, C., Anja, H., Thomas, L., John, R.L., James, S., Jens, S., Jason, R., Zhu, Y.G., Topp, E., 2015. Ecotoxicological assessment of antibiotics: A call for improved consideration of microorganisms. Environment International85, 189–205.

[4] Chen, M., Qiu, T., Sun, Y., Song, Y., Wang, X., Gao, M., 2019. Diversity of tetracycline- and erythromycin-resistant bacteria in aerosols and manures from four types of animal farms in China. Environmental Science and Pollution Research International26, 24213–24222.

[5] Chi, S.L., Xu, W.H., Han, Y.R., 2022. ARGs distribution and high-risk ARGs identification based on continuous application of manure in purple soil. Science of the Total Environment853, 158667.

[6] D’Costa, V.M., King, C.E., Kalan, L., Morar, M., Sung, W.W.L., Schwarz, C., Froese, D., Zazula, G., Calmels, F., Debruyne, R., Golding, G.B., Poinar, H.N., Wright, G.D., 2011. Antibiotic resistance is ancient. Nature477, 457–461.

[7] Ezzeddin, N., Kalantari, N., Veysi, Z., 2022. Perceived social support is greater among food secure Iranian households during the COVID-19 outbreak. Nutrition & Food Science52, 670–683.

[8] Faucon, M.P., Houben, D., Lambers, H., 2017. Plant functional traits: soil and ecosystem services. Trends in Plant Science22, 385–394.

[9] Ho, Y.B., Zakaria, M.P., Latif, P.A., Saari, N., 2012. Simultaneous determination of veterinary antibiotics and hormone in broiler manure, soil and manure compost by liquid chromatography-tandem mass spectrometry. Journal of Chromatography A1262, 160–168.

[10] Huang, H., Chen, Y., Zheng, X., Su, Y., Wan, R., Yang, S., 2016. Distribution of tetracycline resistance genes in anaerobic treatment of waste sludge: The role of pH in regulating tetracycline resistant bacteria and horizontal gene transfer. Bioresource Technology218, 1284–1289.

[11] Jechalke, S., Kopmann, C., Rosendahl, I., Groeneweg, J., Weichelt, V., Krogerrecklenfort, E., Brandes, N., Nordwig, M., Ding, G.C., Siemens, J., Heuer, H., Smalla, K., 2013. Increased abundance and transferability of resistance genes after field application of manure from sulfadiazine-treated pigs. Applied and Environmental Microbiology79, 1704–1711.

[12] Kümmerer, K., 2009. Antibiotics in the aquatic environment – A review – Part II. Chemosphere75, 435–441.

[13] Li, J.J., Xin, Z.H., Zhang, Y.Z., Chen, J.W., Yan, J.X., Li, H.J., Hu, H.W., 2017. Long-term manure application increased the levels of antibiotics and antibiotic resistance genes in a greenhouse soil. Applied Soil Ecology121, 193–200.

[14] Li, Y.M., Hu, X.L., Yang, S., Zhou, J.T., Qi, L., Sun, X.N., Fan, M.Y., Xu, S.H., Cha, M.H., Zhang, M.S., Lin, S.B., Liu, S.Q., Hu, D.F., 2018. Comparison between the fecal bacterial microbiota of healthy and diarrheic captive musk deer. Frontiers in Microbiology9, 300.

[15] Lin, H., Chapman, S.J., Freitag, T.E., Kyle, C., Ma, J., Yang, Y., Zhang, Z., 2019. Fate of tetracycline and sulfonamide resistance genes in a grassland soil amended with different organic fertilizers. Ecotoxicology and Environmental Safety170, 39–46.

[16] Mallon, C.A., Le Roux, X., van Doorn, G.S., Dini-Andreote, F., Poly, F., Salles, J.F., 2018. The impact of failure: unsuccessful bacterial invasions steer the soil microbial community away from the invader’s niche. ISME Journal12, 728–741.

[17] Marx, C., Gunther, N., Schubert, S., Oertel, R., Ahnert, M., Krebs, P., Kuehn, V., 2015. Mass flow of antibiotics in a wastewater treatment plant focusing on removal variations due to operational parameters. Science of the Total Environment538, 779–788.

[18] Mei, Z., Xiang, L., Wang, F., Xu, M., Fu, Y., Wang, Z., Hashsham, S.A., Jiang, X., Tiedje, J.M., 2021. Bioaccumulation of Manure-borne antibiotic resistance genes in carrot and its exposure assessment. Environment International157, 106830.

[19] Noorasyikin, M.N., Zainab, M., 2017. PGPR by Bacillus in vetiver grasss root enhance strength of soil-root matrix system toward slope stabilization in Malaysia. Journal of Applied Science and Engineering12, 3051–3054.

[20] Obayomi, O., Seyoum, M.M., Ghazaryan, L., Tebbe, C.C., Murase, J., Bernstein, N., Gillor, O., 2021. Soil texture and properties rather than irrigation water type shape the diversity and composition of soil microbial communities. Applied Soil Ecology161, 103834.

[21] Pan, M., Chu, L.M., 2017. Fate of antibiotics in soil and their uptake by edible crops. Science of the Total Environment 599–600, 599–600

[22] Pang, S., Zhang, J., 2019. Analysis on the specific bacteria of children with Henoch-Schonlein purpura nephritis with syndrome of qi deficiency and blood stasis. China Journal of Traditional Chinese Medicine and Pharmacy34, 2135–2139.

[23] Puckowski, A., Mioduszewska, K., Lukaszewicz, P., Borecka, M., Caban, M., Maszkowska, J., Stepnowski, P., 2016. Bioaccumulation and analytics of pharmaceutical residues in the environment: A review. Journal of Pharmaceutical and Biomedical Analysis127, 232–255.

[24] Qin, Y.Y., Zhang, X.F., Adamowski, J.F., Biswas, A., Holden, N.M., 2021. Grassland grazing management altered soil properties and microbial β-diversity but not α-diversity on the Qinghai-Tibetan Plateau. Applied Soil Ecology167, 104032.

[25] Reza, A.M., Amir, G.S., 2009. Isolation and characterization of medically important aerobic actinomycetes in soil of Iran (2006–2007). Open Microbiology Journal3, 53–57.

[26] Sardar, M.F., Li, H., Zhu, C., Dar, A.A., Zhang, B., Waqas, M.A., 2021a. Differential effects of sulfamethoxazole concentrations on the enzymatic dynamics of aerobic composting. Bioresource Technology336, 125330.

[27] Sardar, M.F., Zhu, C., Geng, B., Huang, Y., Abbasi, B., Zhang, Z., Song, T., Li, H., 2021b. Enhanced control of sulfonamide resistance genes and host bacteria during thermophilic aerobic composting of cow manure. Environmental Pollution275, 116587.

[28] Schierstaedt, J., Jechalke, S., Nesme, J., Neuhaus, K., Sørensen, S.J., Grosch, R., Smalla, K., Schikora, A., 2020. Salmonella persistence in soil depends on reciprocal interactions with indigenous microorganisms. Environmental Microbiology22, 2639–2652.

[29] Song, T.T., Li, H.N., Li, B.X., Yang, J.X., Sardar, M.F., Yan, M.M., Li, L.Y., Tian, Y.L., Xue, S., Zhu, C.X., 2021a. Distribution of antibiotic-resistant bacteria in aerobic composting of swine manure with different antibiotics. Environmental Sciences Europe33, 1–13.

[30] Song, T.T., Zhu, C.X., Li, B.X., Jiang, K.Y., Wang, X.R., Sardar, F.M., Xue, S., Huang, Y.L., Li, H.N., 2021b. Ciprofloxacin causes the greatest bacterial community variation in swine manure composting. Frontiers in Environmental Science9, 786592.

[31] Song, T.T., Zhu, C.X., Li, B.X., Yan, M.M., Li, H.N., 2023. Manure application led to higher antibiotic resistance risk in red soil compared with black soil and fluvo-aquic soil. Journal of Hazardous Materials Advances9, 100209.

[32] Song, T.T., Zhu, C.X., Xue, S., Li, B.X., Ye, J., Geng, B., Li, L.F., Sardar, M.F., Li, N., Feng, S., Li, H.N., 2020. Comparative effects of different antibiotics on antibiotic resistance during swine manure composting. Bioresource Technology315, 123820.

[33] Thakur, M.P., Putten, W.H., Cobben, M.M.P., Kleunen, M., Geisen, S., 2019. Microbial invasions in terrestrial ecosystems. Nature Reviews Microbiology17, 621–631.

[34] Tran, H.T., Lin, C., Bui, X.T., Itayama, T., Dang, B.T., Cheruiyot, N.K., Hoang, H.G., Vu, C.T., 2021. Bacterial community progression during food waste composting containing high dioctyl terephthalate (DOTP) concentration. Chemosphere265, 129064.

[35] Udikovic-Kolic, N., Wichmann, F., Broderick, N.A., Handelsman, J., 2014. Bloom of resident antibiotic-resistant bacteria in soil following manure fertilization. Proceedings of the National Academy of Sciences of the United States of America111, 15202–15207.

[36] Walia, S., Rana, S.W., Maue, D., Rana, J., Kumar, A., Walia, S.K., 2013. Prevalence of multiple antibiotic-resistant Gram-negative bacteria on bagged, ready-to-eat baby spinach. International Journal of Environmental Health Research23, 108–118.

[37] Wang, L., Wang, J., Wang, J., Zhu, L., Yang, L., Yang, R., 2019. Distribution characteristics of antibiotic resistant bacteria and genes in fresh and composted manures of livestock farms. Science of the Total Environment695, 133781.

[38] Wei, H., Ding, S., Qiao, Z., Su, Y., Xie, B., 2020. Insights into factors driving the transmission of antibiotic resistance from sludge compost-amended soil to vegetables under cadmium stress. Science of the Total Environment729, 138990.

[39] Xie, W.Y., Shen, Q., Zhao, F.J., 2017. Antibiotics and antibiotic resistance from animal manures to soil: a review. European Journal of Soil Science69, 181–195.

[40] Xing, J., Wang, H., Brookes, P.C., Salles, J.F., Xu, J., 2019. Soil pH and microbial diversity constrain the survival of E. coli in soil. Soil Biology & Biochemistry128, 139–149.

[41] Xiong, W., Wang, M., Dai, J., Sun, Y., Zeng, Z., 2018. Application of manure containing tetracyclines slowed down the dissipation of tet resistance genes and caused changes in the composition of soil bacteria. Ecotoxicology and Environmental Safety147, 455–460.

[42] Xu, H., Chen, Z.Y., Wu, X.Y., Zhao, L., Wang, N., Mao, A.Q., Ren, A.Q., Luo, Y., 2020. Antibiotic contamination amplifies the impact of foreign antibiotic-resistant bacteria on soil bacterial community. Science of the Total Environment758, 143693.

[43] Yang, Q., Ren, S., Niu, T., Guo, Y., Qi, S., Han, X., Liu, D., Pan, F., 2014. Distribution of antibiotic-resistant bacteria in chicken manure and manure-fertilized vegetables. Environmental Science and Pollution Research International21, 1231–1241.

[44] Yang, Q., Wang, R., Ren, S., Szoboszlay, M., Moe, L.A., 2016a. Practical survey on antibiotic-resistant bacterial communities in livestock manure and manure-amended soil. Journal of Environmental Science and Health. Part B, Pesticides, Food Contaminants, and Agricultural Wastes51, 14–23.

[45] Yang, Q., Zhang, H., Guo, Y., Tian, T., 2016b. Influence of chicken manure fertilization on antibiotic-resistant bacteria in soil and the endophytic bacteria of pakchoi. International Journal of Environmental Research and Public Health13, 662.

[46] Zarei-Baygi, A., Smith, A.L., 2021. Intracellular versus extracellular antibiotic resistance genes in the environment: Prevalence, horizontal transfer, and mitigation strategies. Bioresource Technology319, 124181.

[47] Zhang, J., Sui, Q., Tong, J., Zhong, H., Wang, Y., Chen, M., Wei, Y., 2018. Soil types influence the fate of antibiotic-resistant bacteria and antibiotic resistance genes following the land application of sludge composts. Environment International118, 34–43.

[48] Zhang, L., Gu, J., Wang, X., Sun, W., Yin, Y., Sun, Y., Guo, A., Tuo, X., 2017. Behavior of antibiotic resistance genes during co-composting of swine manure with Chinese medicinal herbal residues. Bioresource Technology244, 252–260.

[49] Zhang, Y., Cheng, D., Zhang, Y., Xie, J., Xiong, H., Wan, Y., Zhang, Y., Chen, X., Shi, X., 2021. Soil type shapes the antibiotic resistome profiles of long-term manured soil. Science of the Total Environment786, 147361.

[50] Zhao, F., Yang, L., Chen, L., Xiang, Q., Li, S., Sun, L., Yu, X., Fang, L., 2019. Soil contamination with antibiotics in a typical peri-urban area in eastern China: Seasonal variation, risk assessment, and microbial responses. Journal of Environmental Sciences (China)79, 200–212.

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