Abstract
Antibiotic contamination in soil has become a major concern worldwide. At present, it is not clear how two co-existed antibiotics with environmentally relevant concentrations would affect soil bacterial community structure, the abundances of antibiotic resistance genes (ARGs) and functional genes, and whether the effects of antibiotics would differ between rhizosphere and bulk soil. We conducted a greenhouse pot experiment to grow maize in a loess soil treated with oxytetracycline (OTC) or sulfadiazine (SDZ) or both at an environmentally relevant concentration (1 mg kg−1) to investigate the effects of OTC and SDZ on the rhizosphere and bulk soil bacterial communities, abundances of ARGs and carbon (C)-, nitrogen (N)-, and phosphorus (P)-cycling functional genes, and on plant growth and plant N and P nutrition. The results show that the effects of environmentally relevant concentrations of OTC and SDZ on bacterial communities and abundances of ARGs and functional genes differ between maize rhizosphere and bulk soil. The effects of two antibiotics resulted in a higher absolute abundances of accA, tet(34), tnpA-04, and sul2 in the rhizosphere soil than in the bulk soil and different bacterial community compositions and biomarkers in the rhizosphere soil and the bulk soil. However, OTC had a stronger inhibitory effect on the abundances of a few functional genes in the bulk soil than SDZ did, and their combination had no synergistic effect on plant growth, ARGs, and functional genes. The role of co-existed OTC and SDZ decreased shoot height and increased root N concentration. The results demonstrate that environmentally relevant concentrations of antibiotics shift soil microbial community structure, increase the abundances of ARGs, and reduce the abundances of functional genes. Furthermore, soil contamination with antibiotics can diminish agricultural production via phytotoxic effects on crops, and combined effects of antibiotics on plant growth and nutrient uptake should be considered.
Similar content being viewed by others
Data availability
Raw sequencing reads that support the findings of this study have been deposited in NCBI Sequence Read Archive with the accession codes PRJNA879125. The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.
References
An X, Chen Q, Zhu D, Su J (2018) Distinct effects of struvite and biochar amendment on the class 1 integron antibiotic resistance gene cassettes in phyllosphere and rhizosphere. Sci Total Environ 631-632:668–676
Bellino A, Lofrano G, Carotenuto M, Libralato G, Baldantoni D (2018) Antibiotic effects on seed germination and root development of tomato (Solanum lycopersicum L.). Ecotoxicol Environ Saf 148:135–141
Berendsen RL, Pieterse CMJ, Bakker P (2012) The rhizosphere microbiome and plant health. Trends Plant Sci 17:478–486
Berg G, Eberl L, Hartmann A (2005) The rhizosphere as a reservoir for opportunistic human pathogenic bacteria. Environ Microbiol 7:1673–1685
Blau K, Jacquiod S, Sørensen SJ, Su JQ, Zhu YG, Smalla K, Jechalke S (2019) Manure and doxycycline affect the bacterial community and its resistome in lettece rhizosphere and bulk soil. Front Microbiol 10:725
Chai YN, Schachtman DP (2022) Root exudates impact plant performance under abiotic stress. Trends Plant Sci 27:80–91
Chaparro JM, Badri DV, Vivanco JM (2014) Rhizosphere microbiome assemblage is affected by plant development. ISME J 8:790–803
Chen QL, An XL, Zhu YG, Su JQ, Gillings MR, Ye ZL, Cui L (2017) Application of struvite alters the antibiotic resistome in soil, rhizosphere, and phyllosphere. Environ Sci Technol 51:8149–8157
Chenssa L, Jechalke S, Ding GC, Pusino A, Mangia NP, Smalla K (2016) The presence of tetracycline in cow manure changes the impact of repeated manure application on soil bacterial communities. Biol Fertil Soils 52:1121–1134
Conde-Cid M, Núñez-Delgado A, Fernández-Sanjurjo MJ, Álvarez-Rodríguez E, Fernández-Calviño D, Arias-Estévez M (2020) Tetracycline and sulfonamide antibiotics in soils: presence, fate and environmental risks. Processes 8:1479
de la Porte A, Schmidt R, Yergeau E, Constant P (2020) A gaseous milieu: extending the boundaries of the rhizosphere. Trends Microbiol 28:536–542
DeVries SL, Zhang P (2016) Antibiotics and the terrestrial nitrogen cycle: a review. Curr Pollut Rep 2:51–67
Ding C, He J (2010) Effect of antibiotics in the environment on microbial populations. Appl Microbiol Biotechnol 87:925–941
Du LF, Liu WK (2012) Occurrence, fate, and ecotoxicity of antibiotics in agro-ecosystems. A review. Agron Sustain Dev 32:309–327
Fang H, Han YL, Yin YM, Pan X, Yu YL (2014) Variations in dissipation rate, microbial function and antibiotic resistance due to repeated introductions of manure containing sulfadiazine and chlortetracycline to soil. Chemosphere 96:51–56
Gaballah MS, Guo J, Hassanein A, Sobhi M, Zheng Y, Philber M, Li B, Sun H, Dong R (2023) Removal performance and inhibitory effects of combined tetracycline, oxytetracycline, sulfadiazine, and norfloxacin on anaerobic digestion process treating swine manure. Sci Total Environ 857:159536
Ghirardini A, Grillini V, Verlicchi P (2020) A review of the occurrence of selected micropollutants and microorganisms in different raw and treated manure - environmental risk due to antibiotics after application to soil. Sci Total Environ 707:136118
Grenni P, Ancona V, Caracciolo AB (2018) Ecological effects of antibiotics on natural ecosystems: a review. Microchem J 136:25–39
Gudiño ME, Blanco-Tourinan N, Arbona V, Gomez-Cadenas A, Blazquez MA, Navarro-Garcia F (2018) beta-lactam antibiotics modify root architecture and indole glucosinolate metabolism in Arabidopsis thaliana. Plant Cell Physiol 59:2086–2098
Guo A, Pan C, Ma J, Bao Y (2020) Linkage of antibiotic resistance genes, associated bacteria communities and metabolites in the wheat rhizosphere from chlorpyrifos-contaminated soil. Sci Total Environ 741:140457
Gupta AP, Neue HU, Singh VP (1993) Phosphorus determination in rice plants containing variable manganese content by the phospho-molybdo-vanadate (yellow) and phosphomolybdate (blue) colorimetric methods. Commun Soil Sci Plant Anal 24:1309–1318
He HH, Wu MM, Su R, Zhang ZK, Chao C, Pneg Q, Dong ZG, Pang JY, Lambers H (2021) Strong phosphorus (P)- zinc (Zn) interactions in a calcareous soil-alfalfa system suggest that rational P fertilization should be considered for Zn biofortification on Zn-deficient soils and phytoremediation of Zn-contaminated soils. Plant Soil 461:119–134
Hillis DG, Fletcher J, Solomon KR, Sibley PK (2011) Effects of ten antibiotics on seed germination and root elongation in three plant species. Arch Environ Contam Toxicol 60:220–232
Hong J, Huang XH, Wang ZK, Luo XZ, Huang SZ, Zheng Z (2022) Combined toxic effects of enrofloxacin and microplastics on submerged plants and epiphytic biofilms in high nitrogen and phosphorus waters. Chemosphere 308:136099
Jechalke S, Heuer H, Siemens J, Amelung W, Smalla K (2014) Fate and effects of veterinary antibiotics in soil. Trends Microbiol 22:536–545
Jorgensen PS, Aktipis A, Brown Z, Carriere Y, Downes S, Dunn RR, Epstein G, Frisvold GB, Hawthorne D, Grohn YT, Gujar GT, Jasovsky D, Klein EY, Klein F, Lhermie G, Mota-Sanchez D, Omoto C, Schluter M, Scott HM et al (2018) Antibiotic and pesticide susceptibility and the Anthropocene operating space. Nat Sustain 1:632–641
Kang Y, Hao Y, Xia D, Shen M, Li Q, Hu J (2017) The effects of pig manure application on the spread of tetracycline resistance in bulk and cucumber rhizosphere soils: a greenhouse experiment. Can J Microbiol 63:563–572
Kemper N (2008) Veterinary antibiotics in the aquatic and terrestrial environment. Ecol Indic 8:1–13
Kopmann C, Jechalke S, Rosendahl I, Groeneweg J, Kroegerrecklenfort E, Zimmerling U, Weichelt V, Siemens J, Amelung W, Heuer H, Smalla K (2013) Abundance and transferability of antibiotic resistance as related to the fate of sulfadiazine in maize rhizosphere and bulk soil. FEMS Microbiol Ecol 83:125–134
Li G, Li H, Leffelaar PA, Shen J, Zhang F (2015) Dynamics of phosphorus fractions in the rhizosphere of fababean (Vicia faba L.) and maize (Zea mays L.) grown in calcareous and acid soils. Crop Pasture Sci 66:1151–1160
Liu Y, Cui EP, Neal AL, Zhang XX, Li ZY, Xiao YT, Du ZJ, Gao F, Fan XY, Hu C (2019) Reducing water use by alternate-furrow irrigation with livestock wastewater reduces antibiotic resistance gene abundance in the rhizosphere but not in the non-rhizosphere. Sci Total Environ 648:12–24
Martinez JL (2008) Antibiotics and antibiotic resistance genes in natural environments. Science 321:365–367
Mulchandani R, Wang Y, Gillbert M, Van Boeckel TP (2022) Global trends in antimicrobial use in food-producing animals: 2020 to 2030. PLOS Global Public Health 3:e0001305
Ollivier J, Schacht D, Kindler R, Groeneweg J, Engel M, Wilke B-M, Kleineidam K, Schloter M (2013) Effects of repeated application of sulfadiazine-contaminated pig manure on the abundance and diversity of ammonia and nitrite oxidizers in the root-rhizosphere complex of pasture plants under field conditions. Front Microbiol 4:00022
Pan M, Chu LM (2016) Phytotoxicity of veterinary antibiotics to seed germination and root elongation of crops. Ecotoxicol Environ Saf 126:228–237
Philippot L, Spor A, Henault C, Bru D, Bizouard F, Jones CM, Sarr A, Maron PA (2013) Loss in microbial diversity affects nitrogen cycling in soil. ISME J 7:1609–1619
Pielach CA, Roberts DP, Kobayashi DY (2008) Metabolic behavior of bacterial biological control agents in soil and plant rhizospheres. Adv Appl Microbiol 65:199–215
Reichel R, Rosendahl I, Peeters ETHM, Focks A, Groeneweg J, Bierl R, Schlichting A, Amelung W, Thiele-Bruhn S (2013) Effects of slurry from sulfadiazine- (SDZ) and difloxacin- (DIF) medicated pigs on the structural diversity of microorganisms in bulk and rhizosphere soil. Soil Biol Biochem 62:82–91
Rocha DC, Rocha CD, Tavares DS, Calado SLD, Gomes MP (2021) Veterinary antibiotics and plant physiology: an overview. Sci Total Environ 767:144902
Roose-Amsaleg C, Laverman AM (2016) Do antibiotics have environmental side-effects? Impact of synthetic antibiotics on biogeochemical processes. Environ Sci Pollut Res 23:4000–4012
Schimel J, Balser TC, Wallenstein M (2007) Microbial stress-response physiology and its implications for ecosystem function. Ecology 88:1386–1394
Shen YK, Ryser ET, Li H, Zhang W (2021) Bacterial community assembly and antibiotic resistance genes in the lettuce-soil system upon antibiotic exposure. Sci Total Environ 778:146255
Sokol NW, Slessarev E, Marschmann GL, Nicolas A, Blazewicz SJ, Brodie EL, Firestone MK, Foley MM, Hestrin R, Hungate BA, Koch BJ, Stone BW, Sullivan MB, Zablocki O, Pett-Ridge J, Consortium LSM (2022) Life and death in the soil microbiome: how ecological processes influence biogeochemistry. Nat Rev Microbiol 20:415–430
Song HL, Zhang C, Lu YX, Li H, Shao Y, Yang YL (2022) Enhanced removal of antibiotics and antibiotic resistance genes in a soil microbial fuel cell via in situ remediation of agricultural soils with multiple antibiotics. Sci Total Environ 829:154406
Song M, Peng K, Jiang L, Zhang D, Song D, Chen G, Xu H, Li Y, Luo C (2020) Alleviated antibiotic-resistant genes in the rhizosphere of agricultural soils with low antibiotic concentration. J Agric Food Chem 68:2457–2466
Spohn M, Widdig M (2017) Turnover of carbon and phosphorus in the microbial biomass depending on phosphorus availability. Soil Biol Biochem 113:53–59
Tasho RP, Shin WT, Cho JY (2018) Acclimatization of Pisum sativum L. grown in soil contaminated with veterinary antibiotics, an attribute of dose hormetic response of root metabolites. Sci Total Environ 635:364–374
Thiele-Bruhn S, Beck IC (2005) Effects of sulfonamide and tetracycline antibiotics on soil microbial activity and microbial biomass. Chemosphere 59:457–465
Toth JD, Feng YC, Dou ZX (2011) Veterinary antibiotics at environmentally relevant concentrations inhibit soil iron reduction and nitrification. Soil Biol Biochem 43:2470–2472
Udikovic-Kolic N, Wichmann F, Broderick NA, Handelsman J (2014) Bloom of resident antibiotic-resistant bacteria in soil following manure fertilization. Proc Natl Acad Sci USA 111:15202–15207
Van Boeckel TP, Brower C, Gilbert M, Grenfell BT, Levin SA, Robinson TP, Teillant A, Laxminarayan R (2015) Global trends in antimicrobial use in food animals. Proc Natl Acad Sci USA 112:5649–5654
Wang JH, Wang LJ, Zhu LS, Wang J (2018) Individual and combined effects of enrofloxacin and cadmium on soil microbial biomass and the ammonia-oxidizing functional gene. Sci Total Environ 624:900–907
Wei X, Wu SC, Nie XP, Yediler A, Wong MH (2009) The effects of residual tetracycline on soil enzymatic activities and plant growth. J Environ Sci Health Part B-Pestic Food Contaminants Agric Wastes 44:461–471
Wepking C, Badgley B, Barrett JE, Knowlton KF, Lucas JM, Minick KJ, Ray PP, Shawver SE, Strickland MS (2019) Prolonged exposure to manure from livestock-administered antibiotics decreases ecosystem carbon-use efficiency and alters nitrogen cycling. Ecol Lett 22:2067–2076
Xu DM, Pan H, Yao JC, Feng YX, Wu PP, Shao K (2020) Stress responses and biological residues of sulfanilamide antibiotics in Arabidopsis thaliana. Ecotoxicol Environ Saf 199:110727
Yang L, Feng YX, Zhang H, Yu XZ (2021) Estimating the synergistic and antagonistic effects of dual antibiotics on plants through root elongation test. Ecotoxicology 30:1598–1609
Yang Q, Zhang J, Zhu K, Zhang H (2009) Influence of oxytetracycline on the structure and activity of microbial community in wheat rhizosphere soil. J Environ Sci 21:954–959
Yergeau E, Sanschagrin S, Maynard C, St-Arnaud M, Greer CW (2014) Microbial expression profiles in the rhizosphere of willows depend on soil contamination. ISME J 8:344–358
Yu B, Wang X, Yu S, Li Q, Zhou Q (2014) Effects of roxithromycin on ammonia-oxidizing bacteria and nitrite-oxidizing bacteria in the rhizosphere of wheat. Appl Microbiol Biotechnol 98:263–272
Yu X, Zhang X, Chen J, Li Y, Liu X, Feng Y, Sun Y (2022) Source, occurrence and risks of twenty antibiotics in vegetables and soils from facility agriculture through fixed-point monitoring and numerical simulation. J Environ Manag 319:115652
Zak DR, Blackwood CB, Waldrop MP (2006) A molecular dawn for biogeochemistry. Trends Ecol Evol 21:288–295
Zhalnina K, Louie KB, Hao Z, Mansoori N, da Rocha UN, Shi SJ, Cho HJ, Karaoz U, Loque D, Bowen BP, Firestone MK, Northen TR, Brodie EL (2018) Dynamic root exudate chemistry and microbial substrate preferences drive patterns in rhizosphere microbial community assembly. Nat Microbiol 3:470–480
Zhang Y, Cheng D, Xie J, Zhang Y, Wan Y, Zhang Y, Shi X (2022) Impacts of farmland application of antibiotic-contaminated manures on the occurrence of antibiotic residues and antibiotic resistance genes in soil: A meta-analysis study. Chemosphere 300:134529
Zhang ZK, He HH, Han T, Tian XM, Pang JY, Lamers H (2023) Soil oxytetracycline alters the effects of phosphate fertilisation and Bacillus amyloliquefaciens on the bacterial community of Medicago sativa rhizosphere. Appl Soil Ecol 187:104861
Zhang ZK, Su R, Chang C, Cheng X, Peng Q, Lambers H, He HH (2021) Effects of oxytetracycline on plant growth, phosphorus uptake, and carboxylates in the rhizosheath of alfalfa. Plant Soil 461:501–515
Zhen L, Gu J, Hu T, Chen Z (2018) Effects of compost containing oxytetracycline on enzyme activities and microbial communities in maize rhizosphere soil. Environ Sci Pollut Res 25:29459–29467
Zhu YG, Johnson TA, Su JQ, Qiao M, Guo GX, Stedtfeld RD, Hashsham SA, Tiedje JM (2013) Diverse and abundant antibiotic resistance genes in Chinese swine farms. Proc Natl Acad Sci USA 110:3435–3440
Zou Y, Lin MX, Xiong WG, Wang M, Zhang JX, Wang MZ, Sun YX (2018) Metagenomic insights into the effect of oxytetracycline on microbial structures, functions and functional genes in sediment denitrification. Ecotoxicol Environ Saf 161:85–91
Funding
This work was financially supported by the National Key R&D Program of China (2021YFD1900700).
Author information
Authors and Affiliations
Contributions
Zekun Zhang: investigation, formal analysis, visualization, writing—original draft. Le Zhao: investigation. Jie Yang: investigation. Jiayin Pang: writing—review and editing. Hans Lambers: writing—review and editing. Honghua He: funding acquisition, conceptualization, methodology, writing—review and editing.
Corresponding author
Ethics declarations
Ethical approval
Not applicable.
Consent to participate
No human participant is involved in this study.
Consent for publication
All authors have read and agreed to publish the manuscript in this version.
Competing interests
The authors declare no competing interests.
Additional information
Responsible Editor: Robert Duran
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Zhang, ., Zhao, L., Yang, J. et al. Effects of environmentally relevant concentrations of oxytetracycline and sulfadiazine on the bacterial communities, antibiotic resistance genes, and functional genes are different between maize rhizosphere and bulk soil. Environ Sci Pollut Res 31, 22663–22678 (2024). https://doi.org/10.1007/s11356-024-32578-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-024-32578-6