Natural detoxification of antibiotics in the environment: A one health perspective

Abstract

The extended concept of one health integrates biological, geological, and chemical (bio-geo-chemical) components. Anthropogenic antibiotics are constantly and increasingly released into the soil and water environments. The fate of these drugs in the thin Earth space (“critical zone”) where the biosphere is placed determines the effect of antimicrobial agents on the microbiosphere, which can potentially alter the composition of the ecosystem and lead to the selection of antibiotic-resistant microorganisms including animal and human pathogens. However, soil and water environments are highly heterogeneous in their local composition; thus the permanence and activity of antibiotics. This is a case of “molecular ecology”: antibiotic molecules are adsorbed and eventually inactivated by interacting with biotic and abiotic molecules that are present at different concentrations in different places. There are poorly explored aspects of the pharmacodynamics (PD, biological action) and pharmacokinetics (PK, rates of decay) of antibiotics in water and soil environments. In this review, we explore the various biotic and abiotic factors contributing to antibiotic detoxification in the environment. These factors range from spontaneous degradation to the detoxifying effects produced by clay minerals (forming geochemical platforms with degradative reactions influenced by light, metals, or pH), charcoal, natural organic matter (including cellulose and chitin), biodegradation by bacterial populations and complex bacterial consortia (including “bacterial subsistence”; in other words, microbes taking antibiotics as nutrients), by planktonic microalgae, fungi, plant removal and degradation, or sequestration by living and dead cells (necrobiome detoxification). Many of these processes occur in particulated material where bacteria from various origins (microbiota coalescence) might also attach (microbiotic particles), thereby determining the antibiotic environmental PK/PD and influencing the local selection of antibiotic resistant bacteria. The exploration of this complex field requires a multidisciplinary effort in developing the molecular ecology of antibiotics, but could result in a much more precise determination of the one health hazards of antibiotic production and release.

Antimicrobial Resistance in the Global Health Network: Known Unknowns and Challenges for Efficient Responses in the 21st Century

“…Actions targeting the reduction of pharmaceuticals in the environment including the design, synthesis, and production of pharmaceuticals [38]. Determine the concentration of selective antibiotics for AMR in local environments [205,217,218]. Determine the impact of drugs in the environment to regulate microbial residue limits (MRLs) [218] 3 .…”

“…Abiotic surfaces are composed of a diversity of materials. The impact of environmental factors on the selection of bacteria on abiotic reservoirs is largely unexplored [38,217].…”

What are the missing pieces needed to stop antibiotic resistance?

“…Close and long‐term permanent interactions (as in pets) facilitate cross‐transmission of clones, suggesting that this might also occur with other animals in low‐income countries where food animals share with humans common environments. The direction of transmission of clonal transfer is a difficult issue; as humans and co‐resident animals might be colonized by common shared source (Muloi et al, 2018 ), favouring a ‘coalescent common microbiota’ (Sun et al, 2020 , Baquero, Coque, Guerra‐Pinto, et al, 2022 ; Baquero, Coque, & Martínez, 2022 ). Under other conditions, animal‐based transmission of antibiotic‐resistant bacteria is linked to some few generalist clones (Sheppard et al, 2018 ) that serve as shuttles of antibiotic resistance by colonizing/infecting both types of hosts.…”

“…In addition, environmental bacteria constitute a reservoir of resistance genes as ctx‐M , oxa‐48 or qnr (see above) that could be potentially transmitted to human‐pathogenic bacteria, The ‘meeting points’ where human‐pathogenic and naturally resistant organisms can be simultaneously present and eventually interchange antibiotic resistance determinants are not well established, but certainly involve the human microbiota and the environmental microbiotas. These microbiomes probably merge on natural microbiotic small particles (measuring less than 2 mm) to which bacteria and other microbes attach, resulting in medium to long‐term colonization (Baquero, Coque, Guerra‐Pinto, et al, 2022 ; Baquero, Coque, & Martínez, 2022 ). Soil and water particles include mineral particles (clay, carbonates, silicates), and organic particles (as fungi, protozoa, phytoplankton, zooplankton and biodetritus resulting from animal and vegetal decomposition, humus).…”

“…The study of the bioavailability and degradation rate of antimicrobial agents in environments with different physicochemical conditions and microbiomes is a field that requires further research (Baquero, Coque, Guerra‐Pinto, et al, 2022 ; Baquero, Coque, & Martínez, 2022 ). Such a knowledge is critical to evaluate the risk of antibiotic pollution influencing the basic biogeochemical cycles on Earth depending on a healthy microbiosphere.…”