Microdiversity Shapes the Seasonal Niche of Prokaryotic Plankton Inhabiting Surface Waters in a Coastal Upwelling System

Abstract

Seasonality of prokaryotic abundance, diversity and community composition was investigated over a 2-year period in a coastal upwelling time-series station. A marked seasonality was found for prokaryotic abundance, peaking during upwelling and upwelling-to-downwelling transition, and decreasing during downwelling. The latter included a deeper mixed layer and a homogeneous water column favouring higher abundance of archaea (i.e., Marine Group II, Candiadatus nitrosopelagicus), SAR406 clade and the group Bacteria_Others including > 400 rare taxa. Upwelling and transition conditions, characterised by enhanced vertical stratification and a marked hydrographic variability, included a community less diverse with core-phylotypes proliferating, i.e., Flavobacteriaceae, Amylibacter and Planktomarina. Physical and biogeochemical variables collectively explained > 40% of the seasonal changes in prokaryotic assemblages. Additionally, fine-tune bacterial features evidenced 'closely related taxa' within particular bacterial phylotypes such as SAR116 clade; certain Flavobacteria belonging to NS2b, NS4 or NS9; members of the family Cryomorphaceae and Marine Group II, displaying seasonal microdiversity patterns. Taken together, seasonal hydrographic forcing induces a shift in the upwelling-driven microbiome providing new insights into the barely explored seasonal niche partitioning of surface prokaryotic communities in such highly productive upwelling systems. These results are of broad interest for understanding ecosystem functioning and forecast the impacts of current environmental change.

Keywords: DNA sequencing; diversity; ecological niche; flow cytometry; prokaryotes (Bacteria and Archaea); seasonality; upwelling.

FIGURE 1

Fortnight averages of the upwelling index (m³ s⁻¹ km⁻¹) at one 1 × 1° grid centred at 44° N, 9° W during the sampling period covering from May 2016 to May 2018. Original data provided by IEO (http://www.indicedeafloramiento.ieo.es/HAltas/). Dots in the line correspond with sampling dates. Colour shadow areas and letters on the top indicate the upwelling, downwelling and transition periods. Dashed line indicates the break among years 2016, 2017 and 2018.

FIGURE 2

Prokaryotic abundance, PA (A), high nucleic acid content prokaryotes abundance in percentage, HNA_A (B) and Synechococcus sp. abundance (C) from subsurface water samples at station E2CO. Letters above the bars indicate the prevailing hydrographic periods: U = upwelling, T = transition and D = downwelling.

FIGURE 3

Seasonal variability of the Shannon diversity index (H′) and estimated ASV richness (S.Chao1) of prokaryotes for the period of study. Letters above the bars indicate the prevailing hydrographic periods: U = upwelling, T = transition, and D = downwelling.

FIGURE 4

Venn diagram of all the prokaryotic communities between environmental events: upwelling, transition and downwelling. Samples were normalised to the minimum number of reads found in one of the samples (25,370 reads). Samples of each environmental event were averaged for each ASV. The Venn diagram illustrates the overlap of prokaryotic ASVs corresponding to upwelling, transition and downwelling events. The numbers in the circles indicate the number of unique ASVs in each event and the shared number of ASVs in the overlapping environmental events.

FIGURE 5

Deviation (in %) from the mean relative abundance of core phylotypes in upwelling, transition and downwelling events. The relative abundance of each event was calculated as the average relative abundance of the upwelling, transition and downwelling months, respectively.

FIGURE 6

(A) Seasonality of Phylum Bacteria closely‐related taxa in the period of study. Graphs with a single ASV display the number of reads in each sample while graphs with two or more ASVs display the relative abundance of each ASV in each sample. Labels denote the ASV ID number. Colour shadow boxes and letters on the bottom indicate the upwelling (red), downwelling (blue) and transition (yellow) periods. (B) Seasonality of Order Flavobacteriales in the period of study. Graphs with a single ASV display the number of reads in each sample while graphs with two or more ASVs display the relative abundance of each ASV in each sample. Labels denote the ASV ID number. Colour shadow boxes and letters on the bottom indicate the upwelling (red), downwelling (blue) and transition (yellow) periods. (C) Seasonality of Phylum Archaea in the period of study. Graphs with a single ASV display the number of reads in each sample while graphs with two or more ASVs display the relative abundance of each ASV in each sample. Labels denote the ASV ID number. Colour shadow boxes and letters on the bottom indicate the upwelling (red), downwelling (blue) and transition (yellow) periods.

FIGURE 7

Heatmap shows correlations among environmental and biological variables, and individual ASVs. The colour gradient indicates positive correlations in blue tones and negative correlations in red tones, while white indicates no correlation. Significant correlations were highlighted with asterisks. Clusters show the aggregation of prokaryotic groups based on their similarity using Euclidian distance.