Abstract

Coastal zones are exposed to various anthropogenic impacts, such as different types of wastewater pollution, e.g., treated wastewater discharges, leakage from sewage systems, and agricultural and urban runoff. These various inputs can introduce allochthonous organic matter and microbes, including pathogens, into the coastal marine environment. The presence of fecal bacterial indicators in the coastal environment is usually monitored using traditional culture-based methods that, however, fail to detect their uncultured representatives. We have conducted a year-around in situ survey of the pelagic microbiome of the dynamic coastal ecosystem, subjected to different anthropogenic pressures to depict the seasonal and spatial dynamics of traditional and alternative fecal bacterial indicators. To provide an insight into the environmental conditions under which bacterial indicators thrive, a suite of environmental factors and bacterial community dynamics were analyzed concurrently. Analyses of 16S rRNA amplicon sequences revealed that the coastal microbiome was primarily structured by seasonal changes regardless of the distance from the wastewater pollution sources. On the other hand, fecal bacterial indicators were not affected by seasons and accounted for up to 34% of the sequence proportion for a given sample. Even more so, traditional fecal indicator bacteria (Enterobacteriaceae) and alternative wastewater-associated bacteria (Lachnospiraceae, Ruminococcaceae, Arcobacteraceae, Pseudomonadaceae and Vibrionaceae) were part of the core coastal microbiome, i.e., present at all sampling stations. Microbial source tracking and Lagrangian particle tracking, which we employed to assess the potential pollution source, revealed the importance of riverine water as a vector for transmission of allochthonous microbes into the marine system. Further phylogenetic analysis showed that the Arcobacteraceae in our data set was affiliated with the pathogenic Arcobacter cryaerophilus, suggesting that a potential exposure risk for bacterial pathogens in anthropogenically impacted coastal zones remains. We emphasize that molecular analyses combined with statistical and oceanographic models may provide new insights for environmental health assessment and reveal the potential source and presence of microbial indicators, which are otherwise overlooked by a cultivation approach.

Highlights

  • The urbanization and economic development of coastal regions has resulted in an increasing pressure on these environments (Hugo, 2011; Neumann et al, 2015)

  • Despite improvements in wastewater quality discharged from wastewater treatment plant (WWTP), the regular detection of wastewater-borne pathogens in the marine environments suggests that fecal pollution remains a problem (Newton et al, 2013; Luna et al, 2016; Carney et al, 2019), especially in coastal areas subjected to diverse point and non-point pollution sources

  • Our results reveal that bacterial indicators of wastewater pollution were not restricted to stations at the vicinity of the wastewater pollution source, but were widely distributed in this coastal ecosystem (Figures 6, 7)

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Summary

Introduction

The urbanization and economic development of coastal regions has resulted in an increasing pressure on these environments (Hugo, 2011; Neumann et al, 2015). Coastal ecosystems are strongly influenced by land–sea fluxes, related to various anthropogenic inputs either from non-point pollution sources (e.g., agricultural drainage water, urban stormwater runoff, atmospheric deposition, sewage from ships, wildlife, leakage from sewage systems) or point pollution sources (e.g., rivers, wastewater outfalls) All these various inputs introduce mixtures of inorganic/organic chemical compounds (Imai et al, 2002; Kontas et al, 2004; Raymond and Spencer, 2015; Wang and Chen, 2018; Malone et al, 2021) and microorganisms, including pathogens (Naidoo and Olaniran, 2013; Buccheri et al, 2019; Numberger et al, 2019), into the coastal marine ecosystems. Wastewater-borne microbial taxa are linked to infections and mass mortalities of different ecologically and economically important marine species (Sutherland et al, 2010; Ziegler et al, 2016)

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