Down the drain: exploring wastewater's role in coastal microbiome transformations

Many coastal ecosystems worldwide are impacted by wastewater discharges, which introduce nutrients, pollutants, and allochthonous microbes that can alter microbiome composition and function. Although the severity and distribution of these impacts vary across regions, their potential consequences for key ecological processes remain a concern. The resilience and functional adaptability of native coastal microbiomes are still poorly understood. To study the immediate ecological impact of wastewater discharge on a coastal seawater microbiome, we conducted short-term microcosm experiments, exposing a coastal microbiome to two types of treated wastewater: (i) unfiltered wastewater containing nutrients, pollutants, and allochthonous microbes; and (ii) filtered wastewater containing only nutrients and pollutants.

By integrating multi-omics and metabolic assays, we show that wastewater-derived organic matter and nutrients (mostly ammonia and phosphate) did not alter the taxonomic composition of the coastal microbiota, but triggered reorganization of metabolic pathways in them. We observed enhanced metabolism of proteins, amino acids, lipids, and carbohydrates, particularly of the lineages Alteromonadales, Rhodobacterales, and Flavobacteriales. Glaciecola (Alteromonadales), a copiotroph with antagonistic traits, significantly contributed to these shifts. Conversely, allochthonous taxa like Legionellales and Pseudomonadales had minimal impact. Elevated phosphorus concentrations resulting from wastewater input reduced the synthesis of proteins linked to scavenging phosphorus from organic phosphorus compounds, including alkaline phosphatase activity in native Rhodobacterales and Flavobacteriales, with important ecological implications for phosphorus-depleted coastal ecosystems. Furthermore, the presence of wastewater caused a decline in relative abundance and metabolic activity of Synechococcus, potentially affecting carbon cycling. Yet, the coastal microbiome rapidly respired wastewater-derived dissolved organic carbon, resulting in bacterial growth efficiencies consistent with global coastal averages.

Our findings highlight the capacity of coastal microbiomes to withstand wastewater discharge, with critical implications for assessment of anthropogenic perturbations in coastal ecosystems. However, wastewater-driven changes in metabolic functions and niche utilization within the autochthonous microbial community, impacting phosphorus cycling and potentially affecting carbon cycling, may have long-term consequences for ecosystem functioning. Video Abstract.