Planktonic eukaryotes in the Chesapeake Bay: contrasting responses of abundant and rare taxa to estuarine gradients

Abstract

Phytoplankton are important drivers of aquatic ecosystem function and environmental health. Their community compositions and distributions are directly impacted by environmental processes and human activities, including in the largest estuary in North America, the Chesapeake Bay. It is crucial to uncover how planktonic eukaryotes play fundamental roles as primary producers and trophic links and sustain estuarine ecosystems. In this study, we investigated the detailed community structure and spatiotemporal variations of planktonic eukaryotes in the Chesapeake Bay across space and time for three consecutive years. A clear seasonal and spatial shift of total, abundant, and rare planktonic eukaryotes was evident, and the pattern recurred interannually. Multiple harmful algal species have been identified in the Bay with varied distribution patterns, such as Karlodinium, Heterosigma akashiwo, Protoperidinium sp., etc. Compared to abundant taxa, rare subcommunities were more sensitive to environmental disturbance in terms of richness, diversity, and distribution. The combined effects of temporal variation (13.3%), nutrient availability (10.0%), and spatial gradients (8.8%) structured the distribution of eukaryotic microbial communities in the Bay. Similar spatiotemporal patterns between planktonic prokaryotes and eukaryotes suggest common mechanisms of adjustment, replacement, and species interaction for planktonic microbiomes under strong estuarine gradients. To our best knowledge, this work represents the first systematic study on planktonic eukaryotes in the Bay. A comprehensive view of the distribution of planktonic microbiomes and their interactions with environmental processes is critical in understanding the underlying microbial mechanisms involved in maintaining the stability, function, and environmental health of estuarine ecosystems.

Importance: Deep sequencing analysis of planktonic eukaryotes in the Chesapeake Bay reveals high community diversity with many newly recognized phytoplankton taxa. The Chesapeake Bay planktonic eukaryotes show distinct seasonal and spatial variability, with recurring annual patterns of total, abundant, and rare groups. Rare taxa mainly contribute to eukaryotic diversity compared to abundant groups, and they are more sensitive to spatiotemporal variations and environmental filtering. Temporal variations, nutrient availability, and spatial gradients significantly affect the distribution of eukaryotic microbial communities. Similar spatiotemporal patterns in prokaryotes and eukaryotes suggest common mechanisms of adjustment, substitution, and species interactions in planktonic microbiomes under strong estuarine gradients. Interannually recurring patterns demonstrate that diverse eukaryotic taxa have well adapted to the estuarine environment with a long residence time. Further investigations of how human activities impact estuarine planktonic eukaryotes are critical in understanding their essential ecosystem roles and in maintaining environmental safety and public health.

Keywords: Chesapeake Bay; abundant and rare taxa; harmful algal species; planktonic eukaryotes; spatiotemporal variations.

Fig 1

Map of the Chesapeake Bay showing sampling stations and the percentages of ASVs that are responsive/nonresponsive to environmental gradients. Pie size is proportional to the relative abundance of those ASVs that respond significantly (P < 0.01) (left) or not (right) to environmental factors at each site. Map was created using Ocean Data View version 5.4.0.

Fig 2

Relative abundance of major eukaryotic taxa in the Chesapeake Bay. Seasonal data (winter, spring, summer, and autumn) from each sampling site for three consecutive years (Y1–Y3) are included (unless it is unavailable). Bubble size represents the relative abundance of each taxon within each sample.

Fig 3

Diversity and richness of eukaryotic microorganisms (ASVs) across seasons in the Chesapeake Bay. Top, all taxa; middle, abundant taxa; and bottom, rare taxa. Different letters indicate significant differences between seasons.

Fig 4

Diversity and richness of eukaryotic microorganisms (ASVs) along salinity gradients in the Chesapeake Bay.

Fig 5

NMDS ordination plots for planktonic eukaryotes across season and space.

Fig 6

RDA ordination for the Chesapeake Bay planktonic eukaryotes in relation to environmental parameters. Only significant explanatory environmental factors (P < 0.05) (blue) and taxa (ASVs) with goodness-of-fit ≥0.38 (black) are included.

Fig 7

Variation partitioning analysis of eukaryotic communities and causing environmental factors in the Chesapeake Bay.