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Specific Desulfuromonas Strains Can Determine Startup Times Of applied sciences Article Specific Desulfuromonas Strains Can Determine Startup Times of Microbial Fuel Cells Keren Yanuka-Golub 1,* , Leah Reshef 2, Judith Rishpon 1,2 and Uri Gophna 1,2 1 The Porter School of Environmental Studies, Tel Aviv University, P.O. Box 39040, Tel Aviv 6997801, Israel; [email protected] (J.R.); [email protected] (U.G.) 2 The Shmunis School of Biomedicine and Cancer Research, Faculty of Life Sciences, Tel Aviv University, Tel Aviv 6997801, Israel; [email protected] * Correspondence: [email protected] Received: 31 October 2020; Accepted: 27 November 2020; Published: 30 November 2020 Abstract: Microbial fuel cells (MFCs) can generate electricity simultaneously with wastewater treatment. For MFCs to be considered a cost-effective treatment technology, they should quickly re-establish a stable electroactive microbial community in the case of system failure. In order to shorten startup times, temporal studies of anodic biofilm development are required, however, frequent sampling can reduce the functionality of the system due to electroactive biomass loss; therefore, on-line monitoring of the microbial community without interfering with the system’s stability is essential. Although all anodic biofilms were composed of Desulfuromonadaceae, MFCs differed in startup times. Generally, a Desulfuromonadaceae-dominated biofilm was associated with faster startup MFCs. A positive PCR product of a specific 16S rRNA gene PCR primer set for detecting the acetate-oxidizing, Eticyclidine (PCE)-dechlorinating Desulfuromonas group was associated with efficient MFCs in our samples. Therefore, this observation could serve as a biomarker for monitoring the formation of an efficient anodic biofilm. Additionally, we successfully enriched an electroactive consortium from an active anode, also resulting in a positive amplification of the specific primer set. Direct application of this enrichment to a clean MFC anode showed a substantial reduction of startup times from 18 to 3 days. Keywords: microbial fuel cells (MFCs); startup time; Desulfuromonadaceae; anodic biofilm; specific 16S-Desulfuromonas primer set 1. Introduction Microbial fuel cells (MFCs) are electrochemical devices that utilize anaerobic electroactive microorganisms to promote generation of electricity as a renewable clean source of energy directly from wastewater, and recently, for bioremediation of contaminated sites [1,2]. The working principle of MFCs is based on the activity of an electrochemically active biofilm that anaerobically oxidizes various organic substrates on the anode surface. The microorganisms that grow on the anode and that are responsible for the electron transfer are usually dissimilatory metal-reducing bacteria that are found ubiquitously in soils due to their ability to reduce insoluble elements, such as iron Fe+3 and manganese Mn+4 oxides [3]. The two best characterized families of dissimilatory metal reducing microorganisms in MFC systems are Geobacteracaea and Shewanellacaea. They differ considerably in metabolic flexibility [4] and in their individual electron transfer mechanisms [5]. Additional species belonging to the Desulfuromonadaceae family are well recognized, yet less studied metal reducers. Desulfuromonas members reduce elemental sulfur to sulfide in order to obtain energy, but can also use fumarate, ferric iron (Fe+3), or manganese (Mn+4) as terminal electron acceptors [6]. Moreover, they can obtain energy from the complete oxidation of organic compounds to carbon dioxide, while reducing Appl. Sci. 2020, 10, 8570; doi:10.3390/app10238570 www.mdpi.com/journal/applsci Appl. Sci. 2020, 10, 8570 2 of 12 extracellular electron acceptors [7]. Therefore, it is not surprising that Desulfuromonas and Geobacter species are so closely related [8] and are often reported to be the most predominate taxa found on MFC anodes. Anodic biofilms may face different, often suboptimal and varying abiotic conditions during their formation and operation, which is a challenge for the operation of MFCs as a cost-effective wastewater treatment technology. Of particular concern is the necessity of real-world MFCs to operate incessantly, as a wastewater plant cannot be shut down in the case of MFC failure. Thus, there is a true need for ways to monitor MFC operation in real time to predict system failure, as well as a means to rapidly restart the system, should such failure occur. Major factors that can limit the electrical output in scaled-up MFCs are directly related to the electroactive microbial community, as well as its electron transport efficiency towards the anode. The anodic biofilm microbial composition has been considered to be a vital component of the MFC performance, and an important parameter for assessing the performance of MFCs and the metabolic processes taking place under different conditions [9–15]. Anodic biofilm enrichment involves specific selection processes that eventually dictate the biofilm community composition at steady state, i.e., when a stable maximal voltage has been obtained. Little is known about the microbial processes that actually stimulate the complex development of an anodic biofilm composition and function. Furthermore, anodic biofilms are often inappropriately considered to have reached the mature phase when a stable voltage output is first obtained, while the microbial community may still be changing at that time [16]. However, achieving this knowledge is difficult given typical MFCs experimental designs that allow anodic biofilm sampling only for limited time points during an experiment, which does not provide a direct linkage between the colonization process of microbial cells and power production. This is because sampling methods usually require sampling a considerable fraction of the biomass which necessitates mechanical disruption of the anode. We recently observed that efficient MFCs had Desulforomodaceae-dominated biofilms, while non-efficient MFCs showed a co-dominance of the anodic biofilm by both Desulfuromonadaceae and Geobacteraceae [17]. These findings led to a better understanding of the important community dynamics that occur during the inoculation phase, and eventually lead to either an efficient or non-efficient MFC. One of the important findings was that members of Desulfuromonadaceae were associated with efficient MFCs, and this association was accelerated when Geabacteraceae members were outcompeted from the MFC by the former group. Thus, there seemed to be strong competitive interactions between Desulfuromonadaceae and Geabacteraceae that strongly affected the startup efficiency of an MFC. Since there were no higher resolution taxonomic assignments of the family Desulfuromonadaceae to genus or species, it was unclear whether there were different species or strains of this family arising in the anodic biofilm at different time points and whether a specific strain within this family group was more strongly associated with MFC efficiency than others. Here, our aim was to detect specific patterns of microbial dynamics that characterize shorter MFC startup times, focusing on Desulfuromonadaceae strains using a specific Desulfuromonas-targeted PCR primer set. Furthermore, direct application of a Desulfuromonas-enriched consortium was attempted in order to substantially reduce startup times relative to those observed by inoculating MFCs with a wastewater sample alone. 2. Materials and Methods 2.1. MFC Setup and Experimental Design Single-chamber, air-cathode MFCs were used for the enrichment of anodic respiring bacteria and suspended-cells (plankton) communities. The MFC was a bottle-type reactor (Adams & Chittenden Scientific Glass Ltd., Berkeley, Canada), 160 mL in capacity, with anode electrodes made of carbon felt 2 2 3 with a surface area of 32.64 cm (providing a specific surface area of 20 m m− ). In every MFC reactor, two identical pieces of carbon felt were attached together and suspended at the center of the bottle. An air cathode was placed at the side port (circular), providing a specific surface 2 3 area of 8 m m− (manganese-based catalyzed carbon commercial E4A electrode with a polypropylene Appl. Sci. 2020, 10, 8570 3 of 12 microporous separator, Electric Fuel Ltd., Bet Shemesh, Israel). The anode and cathode of all close circuit MFCs were connected by Ti wires and an external resistor (1000 W). Voltage across the resistor was monitored at 5 min intervals using a computerized data acquisition system connected to a PC. Before the experiment began, all MFC bottles were thoroughly washed with diluted hydrochloric acid and ultrapure water (Milli-Q system, Millipore, Merck, Rosh-Ha’ayin, Israel), and then autoclaved for 30 min at 121 ◦C. The carbon felt anodes were immersed in 100% ethanol (Merck, Israel) overnight and rinsed with ultrapure water before being placed into the reactor. In this study, four experiments were conducted similarly in terms of all parameters indicated above. Out of the four, three replicate experimental sets (named 2015, 2016, and 2016-2) were inoculated similarly using a diluted wastewater sample (10% v/v of total reactor volume) as the microbial source. For experiment 2015, a sample was taken in March 2015. For experiment 2016, a sample was taken in February 2016, and finally for 2016-2, a wastewater sample was taken in September 2016. The fourth experimental set (2016-E) aimed to directly apply an enriched electroactive consortium (composed of >50% Desulfuromonas spp.) from an active-operating MFC. The consortium was directly applied onto a clean anode in an MFC inoculated with a wastewater sample.
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