Dataset Information

Changes in Bacterioplankton Communities Resulting From Direct and Indirect Interactions With Trace Metal Gradients in an Urbanized Marine Coastal Area.

ABSTRACT: Unraveling the relative importance of both environmental conditions and ecological processes regulating bacterioplankton communities is a central goal in microbial ecology. Marine coastal environments are among the most urbanized areas and as a consequence experience environmental pressures. The highly anthropized Toulon Bay (France) was considered as a model system to investigate shifts in bacterioplankton communities along natural and anthropogenic physicochemical gradients during a 1-month survey. In depth geochemical characterization mainly revealed strong and progressive Cd, Zn, Cu, and Pb contamination gradients between the entrance of the Bay and the north-western anthropized area. On the other hand, low-amplitude natural gradients were observed for other environmental variables. Using 16S rRNA gene sequencing, we observed strong spatial patterns in bacterioplankton taxonomic and predicted function structure along the chemical contamination gradient. Variation partitioning analysis demonstrated that multiple metallic contamination explained the largest part of the spatial biological variations observed, but DOC and salinity were also significant contributors. Network analysis revealed that biotic interactions were far more numerous than direct interactions between microbial groups and environmental variables. This suggests indirect effects of the environment, and especially trace metals, on the community through a few taxonomic groups. These spatial patterns were also partially found for predicted bacterioplankton functions, thus indicating a limited functional redundancy. All these results highlight both potential direct influences of trace metals contamination on coastal bacterioplankton and indirect forcing through biotic interactions and cascading.

SUBMITTER: Coclet C

PROVIDER: S-EPMC6395402 | biostudies-literature | 2019

REPOSITORIES: biostudies-literature

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Changes in Bacterioplankton Communities Resulting From Direct and Indirect Interactions With Trace Metal Gradients in an Urbanized Marine Coastal Area.

Coclet Clément C Garnier Cédric C Durrieu Gaël G Omanović Dario D D'Onofrio Sébastien S Le Poupon Christophe C Mullot Jean-Ulrich JU Briand Jean-François JF Misson Benjamin B

Frontiers in microbiology 20190222

Unraveling the relative importance of both environmental conditions and ecological processes regulating bacterioplankton communities is a central goal in microbial ecology. Marine coastal environments are among the most urbanized areas and as a consequence experience environmental pressures. The highly anthropized Toulon Bay (France) was considered as a model system to investigate shifts in bacterioplankton communities along natural and anthropogenic physicochemical gradients during a 1-month su ...[more]

PMID: 30853948

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Project description:Trace metal (TM) contamination in marine coastal areas is a worldwide threat for aquatic communities. However, little is known about the influence of a multi-chemical contamination on both marine biofilm communities' structure and functioning. To determine how TM contamination potentially impacted microbial biofilms' structure and their functions, polycarbonate (PC) plates were immerged in both surface and bottom of the seawater column, at five sites, along strong TM contamination gradients, in Toulon Bay. The PC plates were incubated during 4 weeks to enable colonization by biofilm-forming microorganisms on artificial surfaces. Biofilms from the PC plates, as well as surrounding seawaters, were collected and analyzed by 16S rRNA amplicon gene sequencing to describe prokaryotic community diversity, structure and functions, and to determine the relationships between bacterioplankton and biofilm communities. Our results showed that prokaryotic biofilm structure was not significantly affected by the measured environmental variables, while the functional profiles of biofilms were significantly impacted by Cu, Mn, Zn, and salinity. Biofilms from the contaminated sites were dominated by tolerant taxa to contaminants and specialized hydrocarbon-degrading microorganisms. Functions related to major xenobiotics biodegradation and metabolism, such as methane metabolism, degradation of aromatic compounds, and benzoate degradation, as well as functions involved in quorum sensing signaling, extracellular polymeric substances (EPS) matrix, and biofilm formation were significantly over-represented in the contaminated site relative to the uncontaminated one. Taken together, our results suggest that biofilms may be able to survive to strong multi-chemical contamination because of the presence of tolerant taxa in biofilms, as well as the functional responses of biofilm communities. Moreover, biofilm communities exhibited significant variations of structure and functional profiles along the seawater column, potentially explained by the contribution of taxa from surrounding sediments. Finally, we found that both structure and functions were significantly distinct between the biofilm and bacterioplankton, highlighting major differences between the both lifestyles, and the divergence of their responses facing to a multi-chemical contamination.

Project description:Bacterioplankton are fundamental components of marine ecosystems and influence the entire biosphere by contributing to the global biogeochemical cycles of key elements. Yet, there is a significant gap in knowledge about their diversity and specific activities, as well as environmental factors that shape their community composition and function. Here, the distribution and diversity of surface bacterioplankton along the coastline of the Gulf of Naples (GON; Italy) were investigated using flow cytometry coupled with high-throughput sequencing of the 16S rRNA gene. Heterotrophic bacteria numerically dominated the bacterioplankton and comprised mainly Alphaproteobacteria, Gammaproteobacteria, and Bacteroidetes Distinct communities occupied river-influenced, coastal, and offshore sites, as indicated by Bray-Curtis dissimilarity, distance metric (UniFrac), linear discriminant analysis effect size (LEfSe), and multivariate analyses. The heterogeneity in diversity and community composition was mainly due to salinity and changes in environmental conditions across sites, as defined by nutrient and chlorophyll a concentrations. Bacterioplankton communities were composed of a few dominant taxa and a large proportion (92%) of rare taxa (here defined as operational taxonomic units [OTUs] accounting for <0.1% of the total sequence abundance), the majority of which were unique to each site. The relationship between 16S rRNA and the 16S rRNA gene, i.e., between potential metabolic activity and abundance, was positive for the whole community. However, analysis of individual OTUs revealed high rRNA-to-rRNA gene ratios for most (71.6% ± 16.7%) of the rare taxa, suggesting that these low-abundance organisms were potentially active and hence might be playing an important role in ecosystem diversity and functioning in the GON.IMPORTANCE The study of bacterioplankton in coastal zones is of critical importance, considering that these areas are highly productive and anthropogenically impacted. Their richness and evenness, as well as their potential activity, are very important to assess ecosystem health and functioning. Here, we investigated bacterial distribution, community composition, and potential metabolic activity in the GON, which is an ideal test site due to its heterogeneous environment characterized by a complex hydrodynamics and terrestrial inputs of varied quantities and quality. Our study demonstrates that bacterioplankton communities in this region are highly diverse and strongly regulated by a combination of different environmental factors leading to their heterogeneous distribution, with the rare taxa contributing to a major proportion of diversity and shifts in community composition and potentially holding a key role in ecosystem functioning.

Dataset Information

Changes in Bacterioplankton Communities Resulting From Direct and Indirect Interactions With Trace Metal Gradients in an Urbanized Marine Coastal Area.

Publications

Changes in Bacterioplankton Communities Resulting From Direct and Indirect Interactions With Trace Metal Gradients in an Urbanized Marine Coastal Area.

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