Direct interspecies electron transfer in anaerobic digestion: Research and technological application

<p indent="0mm">Anaerobic digestion (AD), an economical and eco-friendly strategy for renewable energy recovery, has been widely investigated and applied in the stabilization of various organic wastes. However, two major factors involved in the slow fermentation rate and low methane conversion efficiency still limit its large-scale applications around the world. Methane formation via conventional methanogenic pathway in AD undergoes the three stages: Hydrolysis/acidogenesis, acetogenesis and methanogenesis. The structure of some saccharide- and protein-like organic compounds contained in complex organic waste is relatively complex and stable, limiting the rate of converting them into amino acids, fatty acids and alcohols by fermentative bacteria. Therefore, the hydrolysis/acidogenesis is widely recognized as a rate-limiting step of AD in practical applications. On the other hand, the obligate anaerobic methanogens can only utilize methanol, methylamine, formate, acetate and hydrogen/carbon dioxide as substrates. Methane formation with amino acids, fatty acids and alcohols as substrates requires the essential conversion of them into acetate and hydrogen/carbon dioxide by acetogenic bacteria, and then depends on acetate- and hydrogen-utilizing methanogens to metabolize acetate and hydrogen/carbon dioxide into methane, respectively. This working mode of syntrophic metabolism of organic compounds into methane between acetogenic bacteria and methanogens that depends on hydrogen as an interspecies electron carrier has been widely described as Interspecies Hydrogen Transfer (IHT). Formate may be also served as a substitute for hydrogen as an interspecies electron carrier (Interspecies Formate Transfer, IFT). Syntrophic metabolism of organic compounds is strictly limited by the hydrogen partial pressure, since the oxidation of organic compounds into acetate with H⁺ as an electron acceptor is not feasible in thermodynamics (<inline-formula id="INLINE4"><mml:math xmlns:mml="http://www.w3.org/1998/Math/MathML" display="inline"><mml:mrow><mml:msub><mml:mrow other="0"><mml:mi other="0">E</mml:mi></mml:mrow><mml:mrow other="1"><mml:msup other="1"><mml:mrow other="1"><mml:mstyle mathvariant="normal" other="1"><mml:mrow other="1"><mml:mi other="1">H</mml:mi></mml:mrow></mml:mstyle></mml:mrow><mml:mrow other="2"><mml:mo other="2">+</mml:mo></mml:mrow></mml:msup><mml:mo other="1">/</mml:mo><mml:msub other="1"><mml:mstyle mathvariant="normal" other="1"><mml:mrow other="1"><mml:mi other="1">H</mml:mi></mml:mrow></mml:mstyle><mml:mrow other="2"><mml:mn other="2">2</mml:mn></mml:mrow></mml:msub></mml:mrow></mml:msub></mml:mrow></mml:math></inline-formula>=<sc>−0.414 V,</sc> pH 7). Syntrophic metabolism via IHT functions well as long as the hydrogen-utilizing methanogens continuously maintain the hydrogen partial pressure low enough (&lt;10⁻⁴−10⁻⁵ atm) that the formation of hydrogen is thermodynamically favorable. Once the metabolic activity of hydrogen-utilizing methanogens is inhibited by the environmental disturbances, such as temperature, pH or organic loading rate (OLR), they will fail to effectively consume hydrogen. Consequently, syntrophic metabolism of organic compounds will be prevented, causing the accumulation of fatty acids and alcohols that further destroys the acidic balance of system and inhibits the methanogenesis. In 2014, the researchers in University of Massachusetts, Amherst proposed a novel methanogenic pathway, direct interspecies electron transfer (DIET)-based methanogenic pathway. DIET-based methanogenic pathway can avoid the conventional hydrolysis/acidification-methanogenesis, and no longer requires H₂ as an interspecies electron carrier, which is expected to break through the rate limitation of hydrolysis of complex organics and the thermodynamic barrier of producing acetate. DIET-based methanogenic pathway challenges the long-held viewpoint that, methane formation with complex organic compounds in conventional AD requires the initial conversion of them into amino acids, fatty acids and alcohols via the slow hydrolysis/acidogenesis by fermentative bacteria, as well as syntrophic metabolism of these substrates between acetogenic bacteria and methanogens depends on H₂ as a primary electron carrier. Recently, researchers systematically illustrated the fundamental mechanisms, key microbial players and effectiveness of various conductive additives in the field of DIET. However, to our best knowledge, it is equally important to indicate the research and technological application of DIET-based methanogenic pathway in AD. Therefore, this review summarized the recent advances on DIET-based methanogenic pathway for guiding the future direction, illustrated the DIET-based methanogenic communities and their available substrates for finding more DIET-based syntrophs and methanogens, as well as evaluated the strategies of promoting DIET-based methanogenic pathway for addressing the main challenges and opportunities.