Discharge and Salinity Drive Taxonomic and Functional Turnover of Microbial Communities in a Turbid Macrotidal Estuary

Abstract

Although microorganisms are vital to estuarine ecology, the drivers of spatiotemporal changes in their functional community structure remain poorly understood. Using DNA-amplicon sequencing of the V1-V3 and V4 regions of the 16S rRNA and 18S rRNA gene, respectively, we studied the spatiotemporal dynamics of bacterial and eukaryotic microbial communities in the freshwater and brackish tidal reaches of the Schelde estuary (Belgium) from 2018 to 2021. Our analyses revealed pronounced seasonal and longitudinal turnover in autotrophic and heterotrophic microbiota, mainly driven by changes in freshwater discharge, which in turn modulate the salinity and turbidity gradient. Higher discharge in early spring led to a more uniform community composition across the estuary, with higher relative abundances of heterotrophic eukaryotes. As discharge decreased in late spring, the salinity gradient and associated turnover in community composition became more accentuated, with Actinomycetota and diatoms dominating the upstream reaches, and ciliates, fungi and marine bacteria being relatively more important downstream from the maximum turbidity zone (MTZ). The high taxonomic resolution of the metabarcoding approach revealed previously undetected fine-scale seasonal and spatial turnover patterns in (semi)cryptic phytoplankton taxa in the estuary (e.g. in the diatoms Cyclotella and Thalassiosira). In addition, we were able to detect for the first time specific spatio-temporal changes in parasitism possibly related to the termination of the phytoplankton bloom.  High discharge due to exceptionally heavy rainfall in July 2021 resulted in the disruption of the summer MTZ and phytoplankton bloom, more downstream spreading of freshwater species and a decline in brackish and polyhaline species.

Keywords: metabarcoding, 16S, 18S, monitoring, Bacteria, protist