Habitat Heterogeneity and Connectivity: Effects on the Planktonic Protist Community Structure at Two Adjacent Coastal Sites (the Lagoon and the Gulf of Venice, Northern Adriatic Sea, Italy) Revealed by Metabarcoding.

Fabrizio Bernardi Aubry,Mauro Bastianini,Simona Armeli Minicante,Roberta Piredda,Grazia Marina Quero,Adriana Zingone,Alessandra Pugnetti,Stefania Finotto

doi:10.3389/fmicb.2019.02736

Fabrizio Bernardi Aubry, Mauro Bastianini + Show 6 more

Open Access

https://doi.org/10.3389/fmicb.2019.02736

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Abstract

The Lagoon of Venice (LoV) and the Gulf of Venice (GoV), two adjacent coastal Long Term Ecological Research (LTER) sites in the northern Adriatic Sea, represent a transitional/marine coupled ecosystem under the influence of regional and local factors. In this study, these sites were sampled on four dates from April 2016 to February 2017 for environmental DNA and relevant abiotic variables, aiming to assess the relative importance of habitat heterogeneity and connectivity in structuring the protist community. High Throughput Sequencing of V4-18S rRNA gene from 56 samples collected at seven stations produced ca 6 million reads, grouped into 7,336 Operational Taxonomic Units (OTUs) at 97% similarity, which were affiliated to protists belonging to 34 taxonomic groups. The whole community was dominated by Bacillariophyta, especially in spring-summer in the LoV, and by Dinophyta, mainly in the GoV. Ciliophora, Syndiniales, and Cryptophyceae were the next more abundant groups. The community structure varied across the seasons and was different in the two ecosystems, which shared 96% of the reads but showed a high proportion of OTUs distributed preferentially in one of the two sites (specialists) and a different partitioning of trophic categories. GoV specialists were mainly Dinophyceae (>56%), followed by Syndiniales and Bacillariophyta, while the LoV specialists were distributed among several groups, including Bacillariophyta, Syndiniales, Ciliophora, Cryptophyceae, and Trebouxiophyceae. The main abiotic drivers of the differences between protist communities were salinity and temperature, which however explained a minor part of the variance (17%), pointing at a higher relevance of biotic factors and inter-taxa relationships. This was more evident in the LoV, where the network analysis highlighted a higher number of OTUs’ connections than in the GoV. Overall, the metabarcoding approach allowed to depict the composition of the whole protist community in the lagoon and adjacent coastal waters with high resolution, revealing many taxa so far not reported in the area. In addition, despite no clear barrier to dispersal processes, differences in the relative abundance and temporal variability of local protist communities indicate that environmental heterogeneity, in these adjacent and connected ecosystems, can be strong enough to allow for ecological segregation.

Highlights

Microbial eukaryotes are versatile components of aquatic environments, covering multiple functional roles – from autotrophy to heterotrophy and mixotrophy – and contributing to biogeochemical cycling (Worden et al, 2015; Keeling and del Campo, 2017)
Inorganic nutrient concentrations were generally higher in the Lagoon of Venice (LoV) (DIN: 18.7–43.7 μM; P-PO4: 0.5– 1.1 μM; Si-SiO4: 17.8–38.7 μM) than in the Gulf of Venice (GoV) (DIN: 5.4– 21.8 μM; P-PO4: 0.2–0.3 μM; Si-SiO4: 5.5–14.6 μM), with peaks in November in both sites
The range values recorded in the study period are quite typical for the two areas and in line with the seasonal values recorded during 5 years of time series for each area (Supplementary Table 1)

Summary

Introduction

Microbial eukaryotes are versatile components of aquatic environments, covering multiple functional roles – from autotrophy to heterotrophy (predators, decomposers, parasites) and mixotrophy – and contributing to biogeochemical cycling (Worden et al, 2015; Keeling and del Campo, 2017). Recent technological developments of molecular microbial ecology have expanded our capacity to describe and investigate the community diversity and structure and the biogeography of the single-celled eukaryotes, informally called protists (Caron et al, 2012; Leray and Knowlton, 2016). These molecular approaches have been widely applied in protist studies in different aquatic ecosystems, including inland, oceanic and coastal waters, and extreme environments (e.g., de Vargas et al, 2015; Ainsworth et al, 2017; Zhang et al, 2017; Brannock et al, 2018). Community composition of planktonic protists may differ among offshore (e.g., de Vargas et al, 2015; Malviya et al, 2016), coastal regions (e.g., Bittner et al, 2013; Massana et al, 2015) and water depths (e.g., Pawlowski et al, 2011); further the community may shift over seasons as well as over smaller (days to weeks) time scales (e.g., Berdjeb et al, 2018; Nagarkar et al, 2018)

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