Faecal contamination determines bacterial assemblages over natural environmental parameters within intermittently opened and closed lagoons (ICOLLs) during high rainfall

Abstract

Intermittently closed and opened lakes and lagoons (ICOLLs) provide important ecosystem services, including food provision and nutrient cycling. These ecosystems generally experience low watershed outflow, resulting in substantial fluctuations in physicochemical parameters that are often compounded by anthropogenic contamination, however the patterns in microbiology within these environments remains uncharacterised. Therefore, we aimed to determine how seasonal heterogeneity in the physicochemical parameters, in comparison to faecal contamination, alter the dynamics of bacterial communities inhabiting ICOLLs on the eastern Australian coast. To address these aims, we sampled four ICOLLs on a monthly basis for one year, using 16S rRNA gene amplicon sequencing to monitor patterns in bacterial diversity and qPCR-based methods to measure faecal contamination from humans (sewage), dogs, and birds. Additionally, we used qPCR to monitor patterns of a suite of antibiotic resistance genes (ARGs) including sulI, tetA, qnrS, dfrA1, and vanB. Differences in bacterial community composition were often associated with temporal shifts in salinity, temperature, pH, DO, and fDOM, but following periods of high rainfall, bacterial assemblages in two of four ICOLLs changed in direct response to sewage inputs. Within these ICOLLs, indicator taxa for stormwater identified using the 16S rRNA amplicon sequencing data, as well as markers for sewage and dog faeces, and levels of the antibiotic resistance genes (ARGs) sulI, tetA, and dfrA1 were significantly more abundant after rainfall. Notably many of the stormwater indicator taxa were potential human pathogens including Arcobacter and Aeromonas hydrophilia, which also displayed significant correlations, albeit weak to moderate, with levels of the ARGs sulI, tetA, and dfrA1. This broad-scale shift in the nature of the bacterial community following rainfall will likely lead to a substantial, and perhaps detrimental, divergence in the ecosystem services provided by the bacterial assemblages within these ICOLLs. We conclude that following rainfall events, sewage was a principal driver of shifts in the microbiology of ICOLLs exposed to stormwater, while natural seasonal shifts in the physicochemical parameters controlled bacterial communities at other times. Increased occurrence of intense precipitation events is predicted as a ramification of climate change, which will lead to increased impacts of stormwater and sewage contamination on important ICOLL ecosystems in the future.