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Plant spatial compartmentalization buffers bacteriome structure and function under antibiotic stress

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Abstract

Agricultural antibiotic contamination poses increasing threats to crop productivity and ecosystem stability through disruption of the plant-associated microbiome. While antibiotic impacts on bulk soil and rhizosphere communities are documented, the extent to which spatial compartmentalization across the plant-soil continuum buffers these effects remains poorly understood. Here, we investigated how compartment-specific selective pressures influence bacterial community assembly, functional resilience, and interaction networks under antibiotic stress. Lettuce (Lactuca sativa) was grown under five treatments in a completely randomized greenhouse design: T1 (sulfamethoxazole [SMX], 3 mg kg⁻¹ + manure + plant), T2 (trimethoprim [TMP], 3 mg kg⁻¹ + manure + plant), T3 (manure + plant, antibiotic-free control), T4 (manure only, plant-free control), and T5 (soil only, negative control). Bacterial communities were profiled across bulk soil, rhizosphere, and endosphere compartments using full-length 16 S rRNA gene sequencing. Spatial compartmentalization emerged as the primary driver of bacteriome structure and functional potential, surpassing antibiotic treatment effects across all analytical approaches. PERMANOVA revealed significant compartment-driven community structuring (R² = 0.189, P = 0.001), while treatment effects were non-significant (R² = 0.145, P = 0.116). Endosphere communities exhibited substantially lower alpha diversity than bulk soil and rhizosphere (P = 0.0001), with significant treatment × compartment interactions (P = 0.007). Antibiotic treatments selectively enriched xenobiotic degradation (P = 0.042) and secondary metabolism functions, particularly in bulk soil, without systematically increasing pathogen-associated or resistance-related functions. Network analysis revealed reduced bacterial connectivity under antibiotic pressure, yet cooperative interactions dominated across all treatments. Compositional differential abundance testing (ALDEx2) detected no significantly altered taxa for primary antibiotic contrasts (T1 vs. T3, T2 vs. T3), indicating context-driven rather than antibiotic-driven compositional changes. Functional diversity was significantly structured by compartment (Shannon P = 0.0017; richness P = 0.0039), while core plant-beneficial functions remained stable across treatments, with large effect sizes (Cohen’s d ≥ 0.8) restricted to antibiotic degradation and secondary metabolism pathways. Our findings demonstrate that plant-microbe spatial structuring provides an ecological buffer that maintains core bacteriome functions against pharmaceutical disturbance, preserving plant-beneficial capabilities despite compositional shifts. The selective enrichment of antibiotic degradation pathways suggests potential for microbiome-assisted mitigation of pharmaceutical residues in agricultural systems. These results provide insights for developing compartment-specific microbiome management strategies that integrate with One Health approaches to enhance agricultural resilience under increasing pharmaceutical pressure in agroecosystems.

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Data availability

All sequence data generated in this project is available at NCBI under BioProject ID PRJNA1302662.

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Acknowledgements

O.S.O. acknowledges fellowship support from the Oppenheimer Memorial Trust. Views expressed are those of the authors and not of the funding agencies. The authors would also like to acknowledge the UESM Sequence facility for the sequencing of the microbiomes.

Funding

This work is based on research supported by the International Atomic Energy Agency (D15022[CRP 2308]).

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Authors and Affiliations

  1. Unit for Environmental Sciences and Management, North-West University, Potchefstroom Campus, Private Bag X6001, Potchefstroom, 2520, South Africa

    Caryn Kgokonyane Lenonyane, Karabo Tsholo, Lesego Getrude Molale-Tom, Cornelius Carlos Bezuidenhout & Oluwaseyi Samuel Olanrewaju

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  1. Caryn Kgokonyane Lenonyane
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  2. Karabo Tsholo
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  3. Lesego Getrude Molale-Tom
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  4. Cornelius Carlos Bezuidenhout
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  5. Oluwaseyi Samuel Olanrewaju
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Contributions

C.C.B. and O.S.O. conceived the project and were responsible for the overall direction and planning. C.K.L., K.T., and O.S.O. were involved in conducting the majority of experiments, encompassing greenhouse experiments, sample collection, and DNA extraction. O.S.O. analyzed the sequence data. C.C.B. provided guidance throughout the manuscript writing process. O.S.O., C.C.B., and L.M.T. supervised the study. O.S.O. and K.T. wrote the paper. All authors reviewed the manuscript.

Corresponding authors

Correspondence to
Lesego Getrude Molale-Tom, Cornelius Carlos Bezuidenhout or Oluwaseyi Samuel Olanrewaju.

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The authors declare no competing interests.

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Lenonyane, C.K., Tsholo, K., Molale-Tom, L.G. et al. Plant spatial compartmentalization buffers bacteriome structure and function under antibiotic stress.
Sci Rep (2026). https://doi.org/10.1038/s41598-026-46797-z

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  • DOI: https://doi.org/10.1038/s41598-026-46797-z

Keywords

  • Plant compartments
  • Antibiotic resistance
  • Functional ecology
  • Plant community structure
  • One health

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