https://doi.org/10.1016/j.biortech.2022.126705

Let́s chat: communication between electroactive microorganisms.

Anode respiration-dependent biological nitrogen fixation by Geobacter sulfurreducens

Abstract Light-induced microbial electron transfer has potential for efficient production of value-added chemicals, biofuels and biodegradable materials owing to diversified metabolic pathways. However, most microbes lack photoactive proteins and require synthetic photosensitizers that suffer from photocorrosion, photodegradation, cytotoxicity, and generation of photoexcited radicals that are harmful to cells, thus severely limiting the catalytic performance. Therefore, there is a pressing need for biocompatible photoconductive materials for efficient electronic interface between microbes and electrodes. Here we show that living biofilms of Geobacter sulfurreducens use nanowires of cytochrome OmcS as intrinsic photoconductors. Photoconductive atomic force microscopy shows up to 100-fold increase in photocurrent in purified individual nanowires. Photocurrents respond rapidly (&lt;100 ms) to the excitation and persist reversibly for hours. Femtosecond transient absorption spectroscopy and quantum dynamics simulations reveal ultrafast (~200 fs) electron transfer between nanowire hemes upon photoexcitation, enhancing carrier density and mobility. Our work reveals a new class of natural photoconductors for whole-cell catalysis. 

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Microbial biofilms as living photoconductors due to ultrafast electron transfer in cytochrome OmcS nanowires

Hydrogen gas (H2) is an attractive fuel carrier due to its high specific enthalpy; moreover, it is a clean source of energy because in the combustion reaction with oxygen (O2) it produces water as the only byproduct. The microbial electrolysis cell (MEC) is a promising technology for producing H2 from simple or complex organics present in wastewater and solid wastes. Methanogens and non-archaeal methane (CH4)-producing microorganisms (NAMPMs) often grow in the MECs and lead to rapid conversion of produced H2 to CH4. Moreover, non-archaeal methane production (NAMP) catalyzed by nitrogenase of photosynthetic bacteria was always overlooked. Thus, suppression of CH4 production is required to enhance H2 yield and production rate. This review comprehensively addresses the principles and current state-of-the-art technologies for suppressing methanogenesis and NAMP in MECs. Noteworthy, specific strategies aimed at the inhibition of methanogenic enzymes and nitrogenase could be a more direct approach than physical and chemical strategies for repressing the growth of methanogenic archaea. In-depth studies on the multiomics of CH4 metabolism can possibly provide insights into sustainable and efficient approaches for suppressing metabolic pathways of methanogenesis and NAMP. The main objective of this review is to highlight key concepts, directions, and challenges related to boosting H2 generation by suppressing CH4 production in MECs. Finally, perspectives are briefly outlined to guide and advance the future direction of MECs for production of high-purity H2 based on genetic and metabolic engineering and on the interspecific interactions.

Suppressing Methane Production to Boost High-Purity Hydrogen Production in Microbial Electrolysis Cells.

In natural anoxic environments, anoxygenic photosynthetic bacteria fix CO2 by photoheterotrophy, photoautotrophy, or syntrophic anaerobic photosynthesis. Here, we describe electroautotrophy, a previously unidentified dark CO2 fixation mode enabled by the electrosyntrophic interaction between Geobacter metallireducens and Rhodopseudomonas palustris. After an electrosyntrophic coculture is formed, electrons are transferred either directly or indirectly (via electron shuttles) from G. metallireducens to R. palustris, thereby providing reducing power and energy for the dark CO2 fixation. Transcriptomic analyses demonstrated the high expression of genes encoding for the extracellular electron transfer pathway in G. metallireducens and the Calvin-Benson-Bassham carbon fixation cycle in R. palustris Given that sediments constitute one of the most ubiquitous and abundant niches on Earth and that, at depth, most of the sedimentary niche is both anoxic and dark, dark carbon fixation provides a metabolic window for the survival of anoxygenic phototrophs, as well as an as-yet unappreciated contribution to the global carbon cycle.

Syntrophic interspecies electron transfer drives carbon fixation and growth by Rhodopseudomonas palustris under dark, anoxic conditions.

The direct conversion of CO2 to value-added chemical commodities, thereby storing solar energy, offers a promising option for alleviating both the current energy crisis and global warming. Semiconductor-biological hybrid systems are novel approaches. However, the inherent defects of photocorrosion, photodegradation, and the toxicity of the semiconductor limit the application of these biohybrid systems. We report here that Rhodopseudomonas palustris was able to directly act as a living photosensitizer to drive CO2 to CH4 conversion by Methanosarcina barkeri under illumination after coculturing. Specifically, R. palustris formed a direct electric syntrophic coculture with M. barkeri. Here, R. palustris harvested solar energy, performed anoxygenic photosynthesis using sodium thiosulfate as an electron donor, and transferred electrons extracellularly to M. barkeri to drive methane generation. The methanogenesis of M. barkeri in coculture was a light-dependent process with a production rate of 4.73 ± 0.23 μM/h under light, which is slightly higher than that of typical semiconductor-biohybrid systems (approximately 4.36 μM/h). Mechanistic and transcriptomic analyses showed that electrons were transferred either directly or indirectly (via electron shuttles), subsequently driving CH4 production. Our study suggests that R. palustris acts as a natural photosensitizer that, in coculture with M. barkeri, results in a new way to harvest solar energy that could potentially replace semiconductors in biohybrid systems.

Light-driven carbon dioxide reduction to methane by Methanosarcina barkeri in an electric syntrophic coculture.

The invention provides a method for driving Methanosarcina to produce methane, which is characterized by comprising the following steps: inoculating Rhodopseudomonas bacteria and Methanosarcina bacteria into a syntrophic culture medium, adding an inorganic electron donor and CO2, and culturing under an illumination condition. According to the method, light energy and inorganic compounds in the nature can be used as driving force to excite the oxygen-free photosynthetic bacteria to oxidize and produce electrons, then the Methanosarcina bacteria utilize the electrons to realize selective CO2 reduction to produce methane, and the process cost is remarkably reduced.

Huang Lingyan

Papers

Syntrophic interspecies electron transfer drives carbon fixation and growth by Rhodopseudomonas palustris under dark, anoxic conditions.

Light-driven carbon dioxide reduction to methane by Methanosarcina barkeri in an electric syntrophic coculture.

Method for driving Methanosarcina to produce methane