Tracking the influence of antibiotics, antibiotic resistomes, and salinity gradient in modulating microbial community assemblage of surface water and the ecological consequences

Significance Antibiotic resistance, driven by antibiotic consumption, is a growing global health threat. Our report on antibiotic use in 76 countries over 16 years provides an up-to-date comprehensive assessment of global trends in antibiotic consumption. We find that the antibiotic consumption rate in low- and middle-income countries (LMICs) has been converging to (and in some countries surpassing) levels typically observed in high-income countries. However, inequities in drug access persist, as many LMICs continue to be burdened with high rates of infectious disease-related mortality and low rates of antibiotic consumption. Our findings emphasize the need for global surveillance of antibiotic consumption to support policies to reduce antibiotic consumption and resistance while providing access to these lifesaving drugs.

Worldwide, antibiotic usage exceeds 100,000 tons per year and there is increasing concern over the fate of these substances. Antibiotics are ubiquitous in the environment and significant concentrations have been detected in fresh waters. In this review, we highlight important aspects of antibiotic pollution in fresh waters: that concentrations of antibiotics in the environment are substantial, that micro-organisms are susceptible to this, that bacteria can evolve resistance in the environment, and that antibiotic pollution affects natural food webs while interacting with other stressors; which taken together poses a number of challenges for environmental scientists. In the literature, we found examples of considerable antibiotic pollution in fresh waters. In the Americas, antibiotic concentrations of up to 15 μg/L have been measured; with higher concentrations reported from European and African studies (over 10 μg/L and 50 μg/L respectively), and in Asian-pacific countries concentrations over 450 μg/L have been detected. While these concentrations might not be deemed harmful to humans, non-target freshwater organisms could be affected by them. Bioassays show that some of the antibiotics found in surface waters affect microbes at concentrations below 10 μg/L. Among the most potent antibiotics are those that prevail in streams and rivers in these concentrations, such as ciprofloxacin. Sub-lethal concentrations might not kill prokaryotes but contribute to increased bacterial resistance and change the composition of single-celled communities, as demonstrated in laboratory experiments. This has implications for the microbial food web (e.g. interactions among and between bacteria and their protozoan consumers) and by extension, larger organisms and ecosystem health. The fact that the effects of antibiotics are extremely context-dependent represents a challenge, particularly for in vitro research. We suggest future research avenues, taking into account food web experiments, antibiotics interacting with one another (and other stressors) and discuss how these can help to answer multi-layered research questions.

Sewage sludge and manure are common soil amendments in crop production; however, their impact on the abundance and diversity of the antibiotic resistome in soil remains elusive. In this study, by using high-throughput sequencing and high-throughput quantitative PCR, the patterns of bacterial community and antibiotic resistance genes (ARGs) in a long-term field experiment were investigated to gain insights into these impacts. A total of 130 unique ARGs and 5 mobile genetic elements (MGEs) were detected and the long-term application of sewage sludge and chicken manure significantly increased the abundance and diversity of ARGs in the soil. Genes conferring resistance to beta-lactams, tetracyclines, and multiple drugs were dominant in the samples. Sewage sludge or chicken manure applications caused significant enrichment of 108 unique ARGs and MGEs with a maximum enrichment of up to 3845 folds for mexF. The enrichment of MGEs suggested that the application of sewage sludge or manure may accelerate the dissemination of ARGs in soil through horizontal gene transfer (HGT). Based on the co-occurrence pattern of ARGs subtypes revealed by network analysis, aacC, oprD and mphA-02, were proposed to be potential indicators for quantitative estimation of the co-occurring ARGs subtypes abundance by power functions. The application of sewage sludge and manure resulted in significant increase of bacterial diversity in soil, Proteobacteria, Acidobacteria, Actinobacteria and Chloroflexi were the dominant phyla (>10% in each sample). Five bacterial phyla (Chloroflexi, Planctomycetes, Firmicutes, Gemmatimonadetes and Bacteroidetes) were found to be significantly correlated with the ARGs in soil. Mantel test and variation partitioning analysis (VPA) suggested that bacterial community shifts, rather than MGEs, is the major driver shaping the antibiotic resistome. Additionally, the co-occurrence pattern between ARGs and microbial taxa revealed by network analysis indicated that four bacterial families might be potential hosts of ARGs. These results may shed light on the mechanism underlining the effects of amendments of sewage sludge or manure on the occurrence and dissemination of ARGs in soil.