Unraveling the Metabolic Potential of Asgardarchaeota in a Sediment from the Mediterranean Hydrocarbon-Contaminated Water Basin Mar Piccolo (Taranto, Italy).

Andrea Firrincieli,Andrea Negroni,Martina Cappelletti,Giulio Zanaroli

doi:10.3390/microorganisms9040859

Abstract

Increasing number of metagenome sequencing studies have proposed a central metabolic role of still understudied Archaeal members in natural and artificial ecosystems. However, their role in hydrocarbon cycling, particularly in the anaerobic biodegradation of aliphatic and aromatic hydrocarbons, is still mostly unknown in both marine and terrestrial environments. In this work, we focused our study on the metagenomic characterization of the archaeal community inhabiting the Mar Piccolo (Taranto, Italy, central Mediterranean) sediments heavily contaminated by petroleum hydrocarbons and polychlorinated biphenyls (PCB). Among metagenomic bins reconstructed from Mar Piccolo microbial community, we have identified members of the Asgardarchaeota superphylum that has been recently proposed to play a central role in hydrocarbon cycling in natural ecosystems under anoxic conditions. In particular, we found members affiliated with Thorarchaeota, Heimdallarchaeota, and Lokiarchaeota phyla and analyzed their genomic potential involved in central metabolism and hydrocarbon biodegradation. Metabolic prediction based on metagenomic analysis identified the malonyl-CoA and benzoyl-CoA routes as the pathways involved in aliphatic and aromatic biodegradation in these Asgardarchaeota members. This is the first study to give insight into the archaeal community functionality and connection to hydrocarbon degradation in marine sediment historically contaminated by hydrocarbons.

Highlights

During the past decades, hydrocarbon cycling in marine and terrestrial anoxic environments has been mostly attributed to nitrate- and sulfate-reducing communities of Delta and Betaproteobacteria catalyzing the oxidation of aliphatic and aromatic hydrocarbons most commonly found in marine sediments under anoxic conditions [1,2,3,4,5,6]
Mar Piccolo microbial community, we have identified members of the Asgardarchaeota superphylum that has been recently proposed to play a central role in hydrocarbon cycling in natural ecosystems under anoxic conditions
Mar Piccolo sediments were described as heavily contaminated with heavy metals at 9 mg/kg sediment, polycyclic aromatic hydrocarbons up to 12.7 mg/kg sediment, and polychlorinated biphenyls (PCB) up to 1.7 mg/kg sediment [15,43,44]

Summary

Introduction

Hydrocarbon cycling in marine and terrestrial anoxic environments has been mostly attributed to nitrate- and sulfate-reducing communities of Delta and Betaproteobacteria catalyzing the oxidation of aliphatic and aromatic hydrocarbons most commonly found in marine sediments under anoxic conditions [1,2,3,4,5,6]. Metagenomic studies revealed that members of the Archaea kingdom, i.e., Archaeoglobus, Bathyarchaeota, and Asgardchaeota, carry the genetic potential to degrade short-chain alkanes, aliphatic and aromatic compounds under anaerobic conditions, suggesting that hydrocarbons degradation might not be restricted to Bacteria lineages [7]. The Asgardarchaeota superphylum showed a surprisingly high diversity of pathways involved in hydrocarbons degradation, revealing that this superphylum members might be crucial contributors to the hydrocarbon cycling in anaerobic environments.

Methods

Results

Conclusion