Multi-compartment impact of micropollutants and particularly antibiotics on bacterial communities using environmental DNA at river basin-level

Abstract

Microbial communities, in particular bacterial assemblies, play pivotal roles in sustaining biogeochemical processes within ecosystems. They are also responsible for the degradation of toxic chemicals, while the development of resistance against antimicrobial drugs jeopardises human health. Bacterial communities respond to environmental conditions with diverse structural and functional changes depending on their compartment (water, biofilm or sediment), type of environmental stress, and type of pollution to which they are exposed. In this study, we combined amplicon sequencing of bacterial 16S rRNA genes from water, biofilm, and sediment samples collected in the anthropogenically impacted River Aconcagua basin (Central Chile, South America), in order to evaluate whether micropollutants alter bacterial community structure and functioning based on the type and degree of chemical pollution. Furthermore, we evaluated the potential of bacterial communities from differently polluted sites to degrade contaminants. Our results show a lower diversity at sites impacted by agriculture and urban areas, featuring high loads of micropollution with pesticides, pharmaceuticals and personal care products as well as industrial chemicals. Nutrients, antibiotic stress, and micropollutant loads explain most of the variability in the sediment and biofilm bacterial community, showing a significant increase of bacterial groups known for their capabilities to degrade various organic pollutants, such as Nistrospira and also selecting for taxa known for antibiotic resistance such as Exiguobacterium and Planomicrobium. Moreover, potential ecological functions linked to the biodegradation of toxic chemicals at the basing level revealed significant reductions in ecosystem-related services in sites affected by agriculture and wastewater treatment plant (WWTP) discharges across all investigated environmental compartments. Finally, we suggest transitioning from simple concentration-based assessments of environmental pollution to more meaningful toxic pressure values in order to comprehensively evaluate the role of micropollutants at the ecological (biodiversity) level. Graphical abstract O_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=80 SRC="FIGDIR/small/587215v1_ufig1.gif" ALT="Figure 1"> View larger version (32K): org.highwire.dtl.DTLVardef@4dfdc9org.highwire.dtl.DTLVardef@50c884org.highwire.dtl.DTLVardef@19c62aforg.highwire.dtl.DTLVardef@12db45_HPS_FORMAT_FIGEXP M_FIG C_FIG HighlightsO_LIMicropollutant mixtures altered bacterial community structure and functioning C_LIO_LIAntibiotic stress correlated significantly with changes in community structure C_LIO_LIReduction of ecological functions related to the degradation of contaminants C_LIO_LIWater, biofilm, and sediments relevant for microbial ecotoxicology C_LI