Are earthworms the victim, facilitator or antidote of antibiotics and antibiotic resistance at the soil-animal-human interface? A One-Health perspective.

The transfer of antibiotics and antibiotic resistance (AR) to the soil systems poses ecological hazards to various organisms, including earthworms. Understanding the complex interactions between earthworms, antibiotics, and AR in the soil system requires a comprehensive assessment. Hence, the present review investigates the behaviour, fate, impacts, and mechanisms involved in the interaction of earthworms with antibiotics and AR. The antibiotics and AR detected in earthworms and their associated media, such as vermicompost, are presented, but several other antibiotics and AR widely detected in soils remain understudied. As receptors and bioassay organisms, earthworms are adversely affected by antibiotics and AR causing (1) acute and chronic toxicity, and (2) emergence of AR in previously susceptible earthworm gut microbiota, respectively. The paper also highlights that, apart from this toxicity, earthworms can also mitigate against antibiotics, antibiotic-resistant bacteria and antibiotic-resistance genes by reducing bacterial diversity and abundance. The behaviour and fate processes, including biodegradation pathways, biomarkers of antibiotics and AR in earthworms, are discussed. In addition, the factors controlling the behaviour and fate of antibiotics and AR and their interactions with earthworms are discussed. Overall, earthworms mitigate antibiotics and AR via various proximal and distal mechanisms, while dual but contradictory functions (i.e., mitigatory and facilitatory) were reported for AR. We recommend that future research based on the One-World-One-Health approach should address the following gaps: (1) under-studied antibiotics and AR, (2) degradation mechanisms and pathways of antibiotics, (3) effects of environmentally relevant mixtures of antibiotics, (4) bio-augmentation in earthworm-based bioremediation of antibiotics, (5) long-term fate of antibiotics and their metabolites, (6) bio-transfers of antibiotics and AR by earthworms, (7) development of earthworm biomarkers for antibiotics and AR, (8) application of earthworm-based bioremediation of antibiotics and AR, (9) cascading ecological impacts of antibiotics and AR on earthworms, and (10) pilot-scale field applications of earthworm-based bioremediation systems.