Highly Contaminated Marine Sediments Can Host Rare Bacterial Taxa Potentially Useful for Bioremediation.

Filippo Dell’Anno,Michael Tangherlini,Adrianna Ianora,Maria Rita Montereali,Cinzia Corinaldesi,Antonio Dell’Anno,Eugenio Rastelli,Luigi Musco,Sergio Balzano,Clementina Sansone,Christophe Brunet

doi:10.3389/fmicb.2021.584850

Abstract

Coastal areas impacted by high anthropogenic pressures typically display sediment contamination by polycyclic aromatic hydrocarbons (PAHs) and heavy metals (HMs). Microbial-based bioremediation represents a promising strategy for sediment reclamation, yet it frequently fails due to poor knowledge of the diversity and dynamics of the autochthonous microbial assemblages and to the inhibition of the target microbes in the contaminated matrix. In the present study, we used an integrated approach including a detailed environmental characterization, high-throughput sequencing and culturing to identify autochthonous bacteria with bioremediation potential in the sediments of Bagnoli-Coroglio (Gulf of Naples, Mediterranean Sea), a coastal area highly contaminated by PAHs, aliphatic hydrocarbons and HMs. The analysis of the benthic prokaryotic diversity showed that the distribution of the dominant taxon (Gammaproteobacteria) was mainly influenced by PAHs, As, and Cd concentrations. The other abundant taxa (including Alphaproteobacteria, Deltaproteobacteria, Bacteroidetes, Acidobacteria, Actinobacteria, NB1-j, Desulfobacterota, and Myxococcota) were mainly driven by sediment grain size and by Cu and Cr concentrations, while the rare taxa (i.e., each contributing <1%) by As and aliphatic hydrocarbons concentrations and by sediment redox potential. These results suggest a differential response of bacterial taxa to environmental features and chemical contamination and those different bacterial groups may be inhibited or promoted by different contaminants. This hypothesis was confirmed by culturing and isolating 80 bacterial strains using media highly enriched in PAHs, only nine of which were contextually resistant to high HM concentrations. Such resistant isolates represented novel Gammaproteobacteria strains affiliated to Vibrio, Pseudoalteromonas, and Agarivorans, which were only scarcely represented in their original assemblages. These findings suggest that rare but culturable bacterial strains resistant/tolerant to high levels of mixed contaminants can be promising candidates useful for the reclamation by bioaugmentation strategies of marine sediments that are highly contaminated with PAHs and HMs.

Highlights

Bioremediation of marine sediments contaminated by polycyclic aromatic hydrocarbons (PAHs) and heavy metals (HMs) is a major priority for coastal areas impacted by industrial activities, wastewater discharge, and other anthropic pressures (BurgosNúñez et al, 2017; Jupp et al, 2017; Mali et al, 2017; Monaco et al, 2017; Dell’Anno et al, 2018)
Fresh sediment sub-aliquots were used for bacterial isolation and identification, while other sediment aliquots stored at −20°C were used for the determination of PAH, HM, and aliphatic hydrocarbon concentrations, grain size and quantity and biochemical composition of the organic matter, and for prokaryotic abundance and diversity
Polycyclic aromatic hydrocarbons once extracted from the sediment samples according to EPA 3545A procedure were analyzed by gas chromatography-mass spectrometry (GC-MS; EPA 8270D)

Summary

Introduction

Bioremediation of marine sediments contaminated by polycyclic aromatic hydrocarbons (PAHs) and heavy metals (HMs) is a major priority for coastal areas impacted by industrial activities, wastewater discharge, and other anthropic pressures (BurgosNúñez et al, 2017; Jupp et al, 2017; Mali et al, 2017; Monaco et al, 2017; Dell’Anno et al, 2018). Fresh sediment sub-aliquots were used for bacterial isolation and identification, while other sediment aliquots stored at −20°C were used for the determination of PAH, HM, and aliphatic hydrocarbon concentrations, grain size and quantity and biochemical composition of the organic matter, and for prokaryotic abundance and diversity.

Results

Conclusion