Elsevier

Bioresource Technology

Volume 254, April 2018, Pages 300-311
Bioresource Technology

Review
Direct interspecies electron transfer via conductive materials: A perspective for anaerobic digestion applications

https://doi.org/10.1016/j.biortech.2018.01.095Get rights and content

Highlights

  • DIET via conductive materials is a promising technology for anaerobic digestion.

  • Critical reviews on current understanding of DIET were conducted.

  • Relevant studies published to date were systematically analyzed.

  • Future perspectives for practical applications are proposed.

Abstract

Anaerobic digestion (AD) is a microbial process that produces renewable energy in the form of methane by treating organic waste and high-strength wastewater. Recent studies have demonstrated that conductive materials can promote direct interspecies electron transfer (DIET) between exoelectrogenic bacteria and methanogenic archaea. DIET via conductive materials is more effective for methane production than interspecies electron transfer using electron carriers such as hydrogen, a principal route of methane production in conventional AD. This critical review presents the current understanding of DIET via conductive materials for methane production, summarizes the relevant studies published to date, and analyzes these studies with regard to conductive materials, substrates, inocula, performance, and microorganisms. Based on this analysis, possible future directions are suggested for practical DIET applications via conductive materials in AD.

Introduction

Anaerobic digestion (AD) involves a series of microbial processes that break down biodegradable matter under anaerobic conditions. AD is often used to treat organic waste (e.g. wastewater sludge and municipal solids wastes) and high-strength wastewater (e.g. livestock wastewater and food wastewater) (Khalid et al., 2011). Compared with aerobic processes, AD has several advantages including low biological solid production, low nutrient requirements, high loading operation, and biogas production (Rittmann and McCarty, 2000). As methane is the main component of biogas (50–70%, (Wang et al., 2017) and has an energy value of 35.8 kJ per liter under standard conditions (Corona and Razo-Flores, 2018), it can be used as an energy source for heating and electricity generation. However, slow reactions, odor production, the requirement of a buffer for maintaining neutral pH, and unsuitability for low-strength wastewater are disadvantages of AD (Rittmann and McCarty, 2000). The slow reaction requires long hydraulic retention times (20–50 days for conventional digesters, (Kashyap et al., 2003)), which results in high capital costs for developing anaerobic digesters. In addition, the slow reaction necessitates long startup times (Ghanimeh et al., 2018) and long recovery times after the digester is disturbed (Cirne et al., 2007). Many studies have focused on overcoming the slow reaction of AD. The majority have attempted to optimize operational conditions (e.g. temperature, pH, organic loading, and retention time) and to pretreat feed wastes (e.g. ultrasound, microwave, high temperature, high pressure, and oxidizing agent treatment). Catalysts such as Fe, Ni, Zn, Mn, Cu, Co, and Mo were also used to accelerate AD (Choong et al., 2016, Wang et al., 2017). Nevertheless, above methods could not fundamentally solve the problem of AD’s slow reaction.

AD is achieved by cooperative interactions between various microorganisms (Lee et al., 2012). Complex organic wastes are initially hydrolyzed into carbohydrates, proteins, and fats. These compounds are then converted into simple sugars, alcohols, amino acids, and fatty acids, and further transformed into acetate and hydrogen. These reactions are mostly performed by fermenting bacteria (Li et al., 2011). The produced acetate and hydrogen are the two main substrates for methanogenic archaea (Shen et al., 2016), although methylated compounds can also serve as substrates (Liu and Whitman, 2008). Acetate-utilizing methanogens (aceticlastic methanogens) produce methane by cleaving acetate into methane and bicarbonate (Fukuzaki et al., 1990), while hydrogen-utilizing methanogens (hydrogenotrophic methanogens) produce methane by oxidizing hydrogen with carbon dioxide as the terminal electron acceptor (Demirel and Scherer, 2008).

Methane formation using hydrogen is a process of electron transfer from fatty acids or alcohols to carbon dioxide. In this process, hydrogen can be regarded as a diffusive electron carrier. As hydrogen is produced by secondary fermenting bacteria (Li and Fang, 2007) and utilized by hydrogenotrophic methanogens, this process is an interspecies electron transfer (IET). Formate also reportedly plays a role similar to that of hydrogen in methane formation (Thiele and Zeikus, 1988). The production of hydrogen from fatty acids or alcohols is only thermodynamically feasible (i.e. ΔG < 0) when hydrogen concentrations are very low (H2 < 10−4 atm, (Logan et al., 2002)). This condition is achieved by the consumption of hydrogen by hydrogenotrophic methanogens (Li et al., 2018). Therefore, syntrophy between hydrogen-producing bacteria and hydrogenotrophic methanogens is essential for their survival (Cord-Ruwisch et al., 1998). In addition, low concentrations of hydrogen limit the methane formation rate during AD (Boone et al., 1989). Thus, IET via hydrogen is assumed to be a “bottleneck” in methane formation (Kato et al., 2012a).

Since 2012, many studies have reported that supplementing with conductive materials (such as granular activated carbon (GAC)) in the cocultures of electron-donating bacteria and electron-accepting methanogenic archaea (Liu et al., 2012, Rotaru et al., 2015) or in the cultures of mixed anaerobic populations (Lee et al., 2016, Xu et al., 2015) promoted IET for methane formation. Several studies (Cheng and Call, 2016, Liu et al., 2012, Lovley, 2017a) have proved that IET was not mediated by diffusive electron carriers (i.e. hydrogen or formate), but by electrons that were directly transferred to methanogenic archaea via conductive materials. Conductive materials are believed to behave like electricity conduits and facilitate IET. Electron transfer between microorganisms without mediating diffusive electron carriers is now referred to as direct interspecies electron transport (DIET). Surprisingly, most of the studies on DIET via conductive materials have found reduced lag times for initiating methane production, enhanced methane production rates, high methane yields, and resistance to inhibitory conditions. These findings suggest that conventional anaerobic digestion can be significantly improved by supplementing with conductive materials.

Although experimental evidence on DIET via conductive materials for methane production has accumulated over the years, important questions have not been clearly answered. To what extent can DIET improve methanogenic performance? What characteristics of conductive materials stimulate DIET for methane production? What microorganisms are responsible for DIET? Without answering above questions, it is difficult to deploy DIET technology on a commercial scale. For these reasons, DIET is yet to be employed in commercial-scale AD plants. The purpose of this study is to summarize and analyze all the results associated with this technology and thus address the above issues by critically reviewing current understanding. Three potential mechanisms of DIET for methane production were initially introduced. Subsequently, conductive materials used for DIET were classified, and methanogenic performance (e.g. lag time, methane production rate, and methane yield) was analyzed both by conductive material types and doses. Microorganisms potentially involved in DIET were also investigated. This paper concludes by providing future research directions for enabling a robust technology associated with DIET via conductive materials.

Section snippets

Mechanisms of DIET

Three types of DIET mechanisms have been identified to date: DIET via conductive pili (Fig. 1(A)), DIET via membrane-bound electron transport proteins (Fig. 1(B)), and DIET via abiotic conductive materials (Fig. 1(C)).

Analyses of the studies on DIET with conductive materials

Table 1 summarizes the studies performed on methanogenic reactors supplemented with conductive materials. Although most studies reported increased methane formation in response to supplementation with conductive materials, only a few studies provided direct evidence of DIET via conductive materials, mostly based on defined cocultures. Many studies revealed indirect evidence of DIET (such as enrichment of Geobacter species) or only reported the effects of supplementation with conductive

Effects of DIET via conductive materials on methanogenic performance

This section compares the lag times, methane formation rates, methane yields, and resistance to unfavorable conditions in the methanogenic reactors supplemented with conductive materials and those without. For the comparisons, relative decreases in lag times and increased methane formation rates and yields were plotted as a function of the dosage of conductive materials in Fig. 2. All analyses were based on the studies that used mixed population inocula, as presented in Table 1.

Microorganisms found in the DIET reactors

To achieve efficient DIET via conductive materials for methane production, two types of microorganisms should be present (Fig. 1(C)). One is electron-donating bacteria (i.e., organics-oxidizing bacteria that can extracellularly release electrons to conductive materials). The other is methane-forming archaea that can reduce carbon dioxide to methane using electrons transferred from the electron-donating bacteria via conductive materials. Table 2 shows the relevant microorganisms and those

Future perspectives for practical AD applications

AD based on DIET via conductive materials has great practical potential as this technology can solve some of the disadvantages of AD such as the long lag time, slow methane formation rate, low methane yield, and vulnerability to unfavorable conditions. However, it will take time for this technology to be deployed in full-scale AD plants. There are several technical difficulties to be overcome before practical application. This section presents some future perspectives.

Conclusions

This review summarized and analyzed the studies about DIET via conductive materials published to date. Based on the research, the factors affecting DIET (e.g. the types of conductive materials and substrates), key microorganisms (e.g. Geobacter and Methanosarcina species), and effects of DIET (e.g. lag times and methane formation rates) were identified. Furthermore, based on analysis of our current understanding, this review presented future perspectives of this technology for practical

Acknowledgements

This study was supported by the KU-KIST Graduate School Project and by the Korea University Grant.

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