ArticlePublisher preview availableLiterature Review

Dynamic interaction of antibiotic resistance between plant microbiome and organic fertilizers: sources, dissemination, and health risks

Authors:
Habib Ullah
Habib Ullah
Habib Ullah
  • This person is not on ResearchGate, or hasn't claimed this research yet.
Sedky Hassan at Sultan Qaboos University
Sedky Hassan
Qi Yang at Lanzhou University
Qi Yang
El-Sayed Salama at Lanzhou University
El-Sayed Salama
Show all 6 authorsHide
Read publisher preview
Download citation
To read the full-text of this research, you can request a copy directly from the authors.

Abstract and Figures

Antibiotic resistance is a global health problem driven by the irrational use of antibiotics in different areas (such as agriculture, animal farming, and human healthcare). Sub-lethal concentrations of antibiotic residues impose selective pressure on environmental, plant-associated, and human microbiome leading to the emergence of antibiotic-resistant bacteria (ARB). This review summarizes all sources of antibiotic resistance in agricultural soils (including manure, sewage sludge, wastewater, hospitals/pharmaceutical industry, and bioinoculants). The factors (such as the physicochemical properties of soil, root exudates, concentration of antibiotic exposure, and heavy metals) that facilitate the transmission of resistance in plant microbiomes are discussed. Potential solutions for effective measures and control of antibiotic resistance in the environment are also hypothesized. Manure exhibits the highest antibiotics load, followed by hospital and municipal WW. Chlortetracycline, tetracycline, and sulfadiazine have the highest concentrations in the manure. Antibiotic resistance from organic fertilizers is transmitted to the plant microbiome via horizontal gene transfer (HGT). Plant microbiomes serve as transmission routes of ARB and ARGS to humans. The ingestion of ARB leads to human health risks (such as ineffectiveness of medication, increased morbidity, and mortality). Graphical abstract
Figures - available from: World Journal of Microbiology and Biotechnology
This content is subject to copyright. Terms and conditions apply.
A preview of this full-text is provided by Springer Nature.
Learn more
Content available from World Journal of Microbiology and Biotechnology
This content is subject to copyright. Terms and conditions apply.
Vol.:(0123456789)
World Journal of Microbiology and Biotechnology (2025) 41:4
https://doi.org/10.1007/s11274-024-04214-5
REVIEW
Dynamic interaction ofantibiotic resistance betweenplant
microbiome andorganic fertilizers: sources, dissemination, andhealth
risks
HabibUllah1· SedkyH.A.Hassan2· QiYang1· El‑SayedSalama3· PuLiu1· XiangkaiLi1
Received: 26 September 2024 / Accepted: 24 November 2024 / Published online: 18 December 2024
© The Author(s), under exclusive licence to Springer Nature B.V. 2024
Abstract
Antibiotic resistance is a global health problem driven by the irrational use of antibiotics in different areas (such as agricul-
ture, animal farming, and human healthcare). Sub-lethal concentrations of antibiotic residues impose selective pressure on
environmental, plant-associated, and human microbiome leading to the emergence of antibiotic-resistant bacteria (ARB).
This review summarizes all sources of antibiotic resistance in agricultural soils (including manure, sewage sludge, wastewa-
ter, hospitals/pharmaceutical industry, and bioinoculants). The factors (such as the physicochemical properties of soil, root
exudates, concentration of antibiotic exposure, and heavy metals) that facilitate the transmission of resistance in plant micro-
biomes are discussed. Potential solutions for effective measures and control of antibiotic resistance in the environment are
also hypothesized. Manure exhibits the highest antibiotics load, followed by hospital and municipal WW. Chlortetracycline,
tetracycline, and sulfadiazine have the highest concentrations in the manure. Antibiotic resistance from organic fertilizers
is transmitted to the plant microbiome via horizontal gene transfer (HGT). Plant microbiomes serve as transmission routes
of ARB and ARGS to humans. The ingestion of ARB leads to human health risks (such as ineffectiveness of medication,
increased morbidity, and mortality).
* El-Sayed Salama
sayed14@hanyang.ac.kr; salama@lzu.edu.cn
* Pu Liu
liupu@lzu.edu.cn
1 Ministry ofEducation Key Laboratory ofCell
Activities andStress Adaptations, School ofLife
Sciences, Lanzhou University, Lanzhou730000, Gansu,
People’sRepublicofChina
2 Department ofBiology, College ofScience, Sultan Qaboos
University, Muscat 123, Muscat, Oman
3 Department ofOccupational andEnvironmental
Health, School ofPublic Health, Lanzhou University,
Lanzhou730000, Gansu, People’sRepublicofChina
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
... This resistome facilitates pathogen colonization of plant roots, hindering growth and nutrient uptake. Resistance genes are transmitted to plant microbiomes via horizontal gene transfer, posing significant risks to crop health [92]. ...
Bioaerosols in Agriculture: A Comprehensive Approach for Sustainable Crop Health and Environmental Balance
Article
Full-text available
  • Apr 2025
Bioaerosols have risen as pivotal constituents of airborne particles. Closely intertwined with the agricultural domain, these particles exert a significant influence on crops through the dissemination of various microorganisms that modulate crop growth dynamics, adaptive responses to environmental stimuli, and the nutritional profile of agricultural products. As the main vector, airborne particles are at the forefront in the transmission of plant pathogens. Therefore, this review explains the main factors influencing their composition in agricultural settings and their spreading. Furthermore, it elucidates the complex bioaerosol-based communication networks, including bacteria–bacteria, bacteria–plant, and plant–plant interactions, mediated by specialized volatile organic compounds (VOCs) released by plants and bacterial volatile compounds (BVCs) produced by bacteria. These compounds play a crucial role in synchronizing stress responses and facilitating adaptive processes. They serve as a pathway for influencing and regulating the behavior of both plants and microorganisms. Delving into their origin and dispersion, we assess the key methods for their collection and analysis while also comparing the strengths and weaknesses of various sampling techniques. The discussion also extends to delineating the roles of such particles in the formation of biodiversity. Central to this discourse is an in-depth exploration of their role in the agricultural context, particularly focusing on their potential utility in forecasting pathogen transmission and subsequent plant diseases. This review also highlights the importance of applying bioaerosol-based strategies in the promotion of sustainable agricultural practices, thus contributing to the advancement of ecological balance and food security, which remains a neglected area in scientific research.
View
... These findings highlight the potential for AMR transmission via the food chain, especially when vegetables are consumed raw, as bacterial attachment to intestinal cells can enhance colonization and evade immune defences (Thomas et al. 2024). The gastrointestinal (GI) tract may function as a niche for resistant endophytic bacteria where bacterial attachment and evasion of immune defence enhance colonization (Ullah et al. 2025). Combined with virulence factors, AMR significantly increases bacterial survival in the GI environment, amplifying health risks. ...
Sludge amended soil induced multidrug and heavy metal resistance in endophytic Exiguobacterium sp. E21L: genomics evidences
Article
Full-text available
  • Mar 2025
  • WORLD J MICROB BIOT
The emergence of multidrug-resistant bacteria in agro-environments poses serious risks to public health and ecological balance. In this study, Exiguobacterium sp. E21L, an endophytic strain, was isolated from carrot leaves cultivated in soil amended with sewage treatment plant-derived sludge. The strain exhibited resistance to clinically relevant antibiotics, including beta-lactams, fluoroquinolones, aminoglycosides, and macrolides, with a high Multi-Antibiotic Resistance Index of 0.88. Whole-genome sequencing revealed a genome of 3.06 Mb, encoding 3894 protein-coding genes, including antimicrobial resistance genes (ARGs) such as blaNDM, ermF, tetW, and sul1, along with heavy metal resistance genes (HMRGs) like czcD, copB, and nikA. Genomic islands carrying ARGs and stress-related genes suggested potential horizontal gene transfer. The strain demonstrated robust biofilm formation, high cell hydrophobicity (> 80%), and significant auto-aggregation (90% at 48 h), correlating with genes associated with motility, quorum sensing, and stress adaptation. Notably, phenotypic assays confirmed survival under simulated gastrointestinal conditions, emphasizing its resilience in host-associated environments. Comparative genomics positioned Exiguobacterium sp. E21L near Exiguobacterium chiriqhucha RW-2, with a core genome of 2716 conserved genes. Functional annotations revealed genes involved in xenobiotic degradation, multidrug efflux pumps, and ABC-type transporters, indicating versatile resistance mechanisms and metabolic capabilities. The presence of ARGs, HMRGs, and MGEs (mobile genetic elements) highlights the potential role of Exiguobacterium sp. E21L as a reservoir for resistance determinants in agricultural ecosystems. These findings emphasized the need for stringent regulations on sludge-based fertilizers and advanced sludge treatment strategies to mitigate AMR risks in agro-environments.
View
Selection of antibiotic-resistant bacterial populations in the dairy cow gut following intramuscular ceftiofur treatment for metritis
Article
Full-text available
  • Sep 2024
  • J DAIRY SCI
Third-generation cephalosporins such as ceftiofur are critically important antibiotics because human pathogens with resistance to these drugs contribute to high mortality rates. These antibiotics are also frequently given to dairy cattle for treating infections, emphasizing the critical role they play in both human and veterinary medicine. To investigate the impact of intramuscular ceftiofur treatment on the concentration of resistant bacteria in the gut, we focused on cows with metritis, a common bacterial infection that frequently requires antibiotic intervention. Twelve cows with metritis (cases) were enrolled and treated with intramuscular ceftiofur for 5 d along with 12 matched healthy cows that were not given ceftiofur (controls). Fecal samples were collected weekly from cows in both the case and control groups for 4 weeks, starting before the treatment of the case group. Five fecal samples per cow were used for analysis (n = 120 samples). The abundance of Gram-negative bacteria was quantified per sample after plating on MacConkey agar, which was also used to quantify the abundance of Gram-negative bacteria with resistance to ceftiofur, ampicillin, and tetracycline. Interestingly, the case cows with metritis had a greater abundance of Gram-negative bacteria than the control cows just before treatment, but no difference in abundance was observed between groups at wk 1–4. The abundance of ceftiofur-resistant Gram-negative bacteria was also similar between the case and control cows immediately before treatment of the cases. However, a significant increase in abundance of ceftiofur-resistant Gram-negative bacteria was observed in the case cows 1-week after treatment that persisted through wk 3. Although the recovery of ampicillin- and tetracycline-resistant bacteria was similar between the 2 groups post-treatment, cases had significantly higher levels of ampicillin-resistant bacteria before treatment. Collectively, these findings demonstrate that intramuscular ceftiofur treatment can affect the abundance of cultivable Gram-negative bacteria and select for ceftiofur-resistant populations that can persist for up to 3 weeks. Judicious use practices are needed to ensure that ceftiofur and other critically important antibiotics are administered only when necessary to minimize the spread of resistance and safeguard public and animal health.
View
Organic fertilization co-selects genetically linked antibiotic and metal(loid) resistance genes in global soil microbiome
Article
Full-text available
  • Jun 2024
Antibiotic resistance genes (ARGs) and metal(loid) resistance genes (MRGs) coexist in organic fertilized agroecosystems based on their correlations in abundance, yet evidence for the genetic linkage of ARG-MRGs co-selected by organic fertilization remains elusive. Here, an analysis of 511 global agricultural soil metagenomes reveals that organic fertilization correlates with a threefold increase in the number of diverse types of ARG-MRG-carrying contigs (AMCCs) in the microbiome (63 types) compared to non-organic fertilized soils (22 types). Metatranscriptomic data indicates increased expression of AMCCs under higher arsenic stress, with co-regulation of the ARG-MRG pairs. Organic fertilization heightens the coexistence of ARG-MRG in genomic elements through impacting soil properties and ARG and MRG abundances. Accordingly, a comprehensive global map was constructed to delineate the distribution of coexistent ARG-MRGs with virulence factors and mobile genes in metagenome-assembled genomes from agricultural lands. The map unveils a heightened relative abundance and potential pathogenicity risks (range of 4-6) for the spread of coexistent ARG-MRGs in Central North America, Eastern Europe, Western Asia, and Northeast China compared to other regions, which acquire a risk range of 1-3. Our findings highlight that organic fertilization co-selects genetically linked ARGs and MRGs in the global soil microbiome, and underscore the need to mitigate the spread of these co-resistant genes to safeguard public health.
View
Role of MIC levels and 23S rRNA mutation sites to clarithromycin in 14-day clarithromycin bismuth quadruple therapy for Helicobacter pylori eradication: A prospective trial in Beijing
Article
Full-text available
  • Apr 2024
Background Rising clarithromycin resistance undermines Helicobacter pylori (H. pylori) treatment efficacy. We aimed to determine clarithromycin's minimum inhibitory concentration (MIC) levels and identify specific mutation sites in the 23S ribosomal subunit (23S rRNA) that predict treatment outcomes in a 14-day regimen of clarithromycin bismuth quadruple therapy (amoxicillin 1g, clarithromycin 500 mg, rabeprazole 10 mg, and colloidal bismuth pectin 200 mg). Materials and methods We included adult H. pylori patients who hadn't previously undergone clarithromycin-based treatment, either as initial or rescue therapy. Exclusions were made for penicillin allergy, recent use of related medications, severe illnesses, or inability to cooperate. Patients underwent a 14-day clarithromycin bismuth quadruple therapy. Gastric mucosa specimens were obtained during endoscopy before eradication. MIC against amoxicillin and clarithromycin was determined using the E-test method. The receiver operating characteristic (ROC) curve helped to find the optimal clarithromycin resistance MIC breakpoint. Genetic sequences of H. pylori 23S rRNA were identified through Sanger Sequencing. (ChiCTR2200061476) Results Out of 196 patients recruited, 92 met the inclusion criteria for the per-protocol (PP) population. The overall intention-to-treat (ITT) eradication rate was 80.00 % (84/105), while the modified intention-to-treat (MITT) and PP eradication rates were 90.32 % (84/93) and 91.30 % (84/92) respectively. No amoxicillin resistance was observed, but clarithromycin resistance rates were 36.19 % (38/105), 35.48 % (33/93), and 34.78 % (33/92) in the ITT, MITT, and PP populations respectively. Compared with the traditional clarithromycin resistance breakpoint of 0.25 μg/mL, a MIC threshold of 12 μg/mL predicted better eradication. Among 173 mutations on 152 sites in the 23S rRNA gene, only the 2143A > G mutation could predict eradication outcomes (p < 0.000). Conclusions Interpretation of elevated MIC values is crucial in susceptibility testing, rather than a binary "susceptible" or "resistant" classification. The 2143A > G mutation has limited specificity in predicting eradication outcomes, necessitating further investigation into additional mutation sites associated with clarithromycin resistance.
View
Antibiotic Resistance in Plant Pathogenic Bacteria: Recent Data and Environmental Impact of Unchecked Use and the Potential of Biocontrol Agents as an Eco-Friendly Alternative
Article
Full-text available
  • Apr 2024
The economic impact of phytopathogenic bacteria on agriculture is staggering, costing billions of US dollars globally. Pseudomonas syringae is the top most phytopathogenic bacteria, having more than 60 pathovars, which cause bacteria speck in tomatoes, halo blight in beans, and so on. Although antibiotics or a combination of antibiotics are used to manage infectious diseases in plants, they are employed far less in agriculture compared to human and animal populations. Moreover, the majority of antibiotics used in plants are immediately washed away, leading to environmental damage to ecosystems and food chains. Due to the serious risk of antibiotic resistance (AR) and the potential for environmental contamination with antibiotic residues and resistance genes, the use of unchecked antibiotics against phytopathogenic bacteria is not advisable. Despite the significant concern regarding AR in the world today, there are inadequate and outdated data on the AR of phytopathogenic bacteria. This review presents recent AR data on plant pathogenic bacteria (PPB), along with their environmental impact. In light of these findings, we suggest the use of biocontrol agents as a sustainable, eco-friendly, and effective alternative to controlling phytopathogenic bacteria.
View
Antimicrobial resistance: Impacts, challenges, and future prospects
Article
Full-text available
  • Mar 2024
Antimicrobial resistance (AMR) is a critical global health issue driven by antibiotic misuse and overuse in various sectors, leading to the emergence of resistant microorganisms. The history of AMR dates back to the discovery of penicillin, with the rise of multidrug-resistant pathogens posing significant challenges to healthcare systems worldwide. The misuse of antibiotics in human and animal health, as well as in agriculture, contributes to the spread of resistance genes, creating a "Silent Pandemic" that could surpass other causes of mortality by 2050. AMR affects both humans and animals, with resistant pathogens posing challenges in treating infections. Various mechanisms, such as enzymatic modification and biofilm formation, enable microbes to withstand the effects of antibiotics. The lack of effective antibiotics threatens routine medical procedures and could lead to millions of deaths annually if left unchecked. The economic impact of AMR is substantial, with projected losses in the trillions of dollars and significant financial burdens on healthcare systems and agriculture. Artificial intelligence is being explored as a tool to combat AMR by improving diagnostics and treatment strategies, although challenges such as data quality and algorithmic biases exist. To address AMR effectively, a One Health approach that considers human, animal, and environmental factors is crucial. This includes enhancing surveillance systems, promoting stewardship programs, and investing in research and development for new antimicrobial options. Public awareness, education, and international collaboration are essential for combating AMR and preserving the efficacy of antibiotics for future generations.
View
View
View
Fate of intracellular and extracellular antibiotic resistance genes in sewage sludge by full-scale anaerobic digestion
Article
  • Aug 2024
Storage tank (ST) is a promising strategy for solid-liquid separation following anaerobic digestion (AD). How ever, little is known regarding the effects of ST on antibiotic resistance genes (ARGs), mobile genetic elements (MGEs), and microbial communities. Therefore, this study first investigated eight typical ARGs (sul1, sul2, tetW, tetA, tetO, tetX, ermF, and ermB) and three MGEs (int1, int2, and tnpA) during full-scale AD of sludge and the liquid and biosolids phases of ST. Following that, intracellular ARGs (iARGs), extracellular polymeric substances (EPS)- associated ARGs, and cell-free ARGs removal were quantified in AD process, which is largely unknown for full- scale AD of sludge. The qPCR results showed that both AD and ST significantly removed ARGs, with ST biosolids showing the highest removal efficiency for the total measured relative (82.27 ± 2.09 %) and absolute (92.38 ± 0.89 %) abundance of ARGs compared to the raw sludge. Proteobacteria, Bacteroidota, Firmicutes and Campilo bacterota were the main potential ARGs hosts in the sludge. Moreover, the results of different ARGs fractions showed that the total relative and absolute abundance of iARGs decreased by 90.12 ± 0.83 % and 79.89 ± 1.41 %, respectively, following AD. The same trend was observed for the abundance of EPS-associated ARGs, while those of cell-free ARGs increased after AD. These results underscore the risk of extracellular ARGs and provided new insights on extracellular ARGs dissemination evaluation.
View
View
View