Cable Bacteria and the Bioelectrochemical Snorkel: The Natural and Engineered Facets Playing a Role in Hydrocarbons Degradation in Marine Sediments

Abstract

The composition and metabolic traits of the microbial communities acting in an innovative bioelectrochemical system were here investigated. The system, known as Oil Spill Snorkel, was recently developed to stimulate the oxidative biodegradation of petroleum hydrocarbons in anoxic marine sediments. Next Generation Sequencing was used to describe the microbiome of the bulk sediment and of the biofilm growing attached to the surface of the electrode. The analysis revealed that sulfur cycling primarily drives the microbial metabolic activities occurring in the bioelectrochemical system. In the anoxic zone of the contaminated marine sediment, petroleum hydrocarbon degradation occurred under sulfate-reducing conditions and was lead by different families of Desulfobacterales (46% of total OTUs). Remarkably, the occurrence of filamentous Desulfubulbaceae, known to be capable to vehicle electrons deriving from sulfide oxidation to oxygen serving as a spatially distant electron acceptor, was demonstrated. Differently from the sediment, which was mostly colonized by Deltaproteobacteria, the biofilm at the anode hosted, at high extent, members of Alphaproteobacteria (59%) mostly affiliated to Rhodospirillaceae family (33%) and including several known sulfur- and sulfide-oxidizing genera. Overall, we showed the occurrence in the system of a variety of electroactive microorganisms able to sustain the contaminant biodegradation alone or by means of an external conductive support through the establishment of a bioelectrochemical connection between two spatially separated redox zones and the preservation of an efficient sulfur cycling.

The Identification of Cable Bacteria Attached to the Anode of a Benthic Microbial Fuel Cell: Evidence of Long Distance Extracellular Electron Transport to Electrodes

“…Cable bacteria filaments may be uniquely able to accept electrons from different sulfur intermediates (as well as other electron donors) at different points along chains of cells, as they both produce and further oxidize sulfur intermediates (Figure 8 ). It is noteworthy that this hypothetical metabolic framework differs from the microbial community network depicted by Matturro et al ( 2017 ) for an engineered system for the treatment of contaminated sediments, called the “oil spill snorkel.” The snorkel consists of a single graphite rod penetrating oxic and anoxic sediments and serving as both anode and cathode. In this electrode configuration, cable bacteria were proposed to perform sulfide oxidation in parallel with the inserted graphite rod; they were not proposed to attach to the electrode (Matturro et al, 2017 ).…”

“…The discovery of long-distance electron transport mediated by filamentous cable bacteria is rapidly changing views of what biological and chemical factors promote redox reactions in aqueous sediments (Vasquez-Cardenas et al, 2015 ). Until now, models of electrogenic sulfur oxidation by cable bacteria have suggested that access to dissolved O 2 or at least was required for the maintainance of their overall metabolic activity (Marzocchi et al, 2014 ; Meysman et al, 2015 ; Matturro et al, 2017 ). The findings of this study indicate that cable bacteria may in fact be facultative anaerobes.…”

Effect of surface nano/micro-structuring on the early formation of microbial anodes with Geobacter sulfurreducens: Experimental and theoretical approaches

“…For around two decades, microbial anodes have been opening up fascinating avenues for a huge number of electrochemical processes [1 3]. Microbial fuel cells (MFCs) were the pioneering systems in which microbial anodes were implemented [4,5] and they have since been the source of numerous innovative technological concepts, such as microbial electrolysis cells for hydrogen production [6,7] metal re covery [8,9], microbial autonomous biosensors [10,11] and a microbial snorkel for environmental bioremediation [12,13].…”

Impact of electrode micro- and nano-scale topography on the formation and performance of microbial electrodes

“…For instance, microbial fuel cells may be appropriate energy production systems when low power is sufficient (Shleev et al, 2015), such as for powering remote sensors (Dewan et al, 2014) and designing autonomous sensors (Di Lorenzo et al, 2009;Pasternak et al, 2017). Simplifying the equipment to design low-cost devices that do not require attendance, such as the electro-microbial snorkel (Erable et al, 2011;Matturro et al, 2017), or focusing on specific environments, such as hypersaline media (Rousseau et al, 2013;Carmona-Martinez et al, 2015;Grattieri and Minteer, 2018) may also open up promising horizons. Furthermore, microbial electrodes have led to fundamental discoveries on the electrochemical link between living organisms and materials (Borole et al, 2011;Shi et al, 2016;Kumar et al, 2017), which may be involved in many natural processes, such as anaerobic digestion (Kato et al, 2012;Liu et al, 2012) and microbially influenced corrosion (Beech and Sunner, 2004;Mehanna et al, 2009a;Kip and van Veen, 2015).…”