Mechanical force has recently emerged as a microbial energy source through direct mechanical-to-electrical energy conversion. However, the flexoelectric effect, a universal mechanoelectrical coupling phenomenon, remains underexplored as an energy source for microbial life. Here, we report a mechanically-driven microbial growth mechanism whereby mechanical energy is converted into electrical energy via the flexoelectric effect of a mineral. This process supports microbial growth in the absence of sunlight and chemical energy sources. Using flexoelectric manganese oxide and electroactive Rhodopseudomonas palustris as a model biohybrid, we demonstrate that mechanical force bends manganese oxide nanosheets to generate free electrical charge. R. palustris captures and utilizes this electrical energy for growth by coupling carbon fixation and denitrification in the absence of chemical electron donors under dark conditions. This pathway is accessible to various electroactive microorganisms and flexoelectric minerals. These findings reveal a noteworthy energy acquisition pathway for microbial survival in energy-limited settings, providing crucial evidence for the diversity of mechanical-to-metabolic coupling in biological processes.
Microbial biofilm-based hydrovoltaic electricity generators (BioHEGs) exemplify low-cost and facile manufacturing platforms for hydrovoltaic energy, albeit with relatively low power output that is unsatisfactory for practical applications. Herein, in situ surface polymerization of polyaniline (PAni) on Shewanella oneidensis (S. o o) is verified to boost the hydrovoltaic performance of the biohybrid system. Notably, the S. o o@PAni BioHEG unit achieves an ultra-high stable power density of ca. 168.6 mW & sdot;m(-2), which outperforms all BioHEGs hitherto documented by an order of magnitude. Specifically, the output voltage and current density of S. o o@PAni BioHEG are significantly enhanced due to the formation of Schottky junctions at the interface between the microbial biofilm and electrode. Moreover, the synergistic effect of extracellular polymeric substances and PAni induces accelerated electron transfer, thereby lowering the electrical resistance in the system. This work unambiguously provides a reliable strategy for advancing the performance of BioHEGs toward more comprehensive and practical scenarios.
Energy supply underpins all life activities on Earth, governing microbial growth and metabolism. For more than a century, the understanding of microbial energy acquisition has been governed by the classical dual paradigm of phototrophy and chemotrophy. Phototrophic microbes capture solar energy via intracellular photosystems, while chemotrophic microbes obtain energy by oxidizing inorganic or organic substrates. This long-standing framework has served as the theoretical foundation of microbiology and supported technological innovations. However, Earth's natural environment is filled with diverse physical fields, including electric, magnetic, thermal, mechanical, hydrovoltaic, and acoustic fields. Field energy, defined as the energy inherent and spatially distributed in physical fields, has long been overlooked in mainstream studies of microbial energy metabolism and regarded only as a growth regulator or stressor. Recent advances reveal that various physical fields can invisibly and continuously mediate microbial energy utilization. Natural ecosystems contain an "invisible energy network" composed of piezoelectric fields in soil pores, coupled geomagnetic-thermal fields in deep-sea sediments, hydrovoltaic fields at water-solid interfaces, and photoelectrons generated by light-excited semiconductor minerals. These discoveries challenge the limitations of the traditional dual-energy model and indicate that microorganisms have evolved previously unrecognized strategies to capture and utilize field energy. Here, we propose field-effect microbiology, an emerging interdisciplinary field integrating microbiology, electrochemistry, geophysics, and nanoscience. It systematically examines field energy-microbe interactions, elucidates key molecular mechanisms for field energy capture, conversion, and utilization, and establishes a theoretical and technological framework for the coevolution of physical fields, microorganisms, and the environment. Fieldeffect microbiology extends the classical phototrophy-chemotrophy framework by establishing field energy as a new bioavailable energy form, emphasizing active and specific microbe-field adaptations, and covering the full chain from energy generation to practical applications. The core mechanisms involve converting diverse field energies into bioavailable field electrons and field holes through photoelectric, piezoelectric, pyroelectric, and hydrovoltaic effects. These energy carriers are transferred to microbial cells via three pathways: direct electron transfer through outer-membrane proteins, indirect transfer mediated by biological or abiotic electron shuttles, and free radical-mediated transfer in oligotrophic environments. Fieldenergy-driven microbial metabolism is widely distributed in illuminated zones, water-cycle interfaces, thermal fluctuation areas, and mechanically disturbed sediments. Field energy supports microbial survival in extreme habitats such as the deep subsurface, hydrothermal vents, and arid regions, expanding the known boundaries of life and providing new insights into early life evolution. Field-effect microbes also mediate global carbon and nitrogen cycles, enhance biodegradation of persistent pollutants, and act as hidden regulators maintaining elemental balance in terrestrial ecosystems. This novel paradigm features multi-field synergy, functional plasticity, and promising application potential, offering low-carbon and high-efficiency strategies for biosynthesis, environmental bioremediation, agricultural microbial regulation, and ecological restoration. However, key challenges remain, including low energy density and conversion efficiency, unclear quantitative microbe-field interaction mechanisms, insufficient in situ tracking technologies for field electron transfer, and difficulties in scaling laboratory systems to real-world applications. Field-effect microbiology bridges the inorganic physical world and organic life, advancing fundamental understanding of microbial energy metabolism and inspiring innovations in environmental and energy biotechnology.
Bio-hydrovoltaic systems, which leverage the energy embedded in water's natural processes, present a promising avenue for sustainable energy production. Despite notable advances in non-living hydrovoltaic systems, research into biological materials remains relatively underdeveloped, leaving their unique advantages and long-term reliability potential largely untapped. This Review presents a comprehensive synthesis of progress in the field, with a particular focus on the evolution from non-living to living hydrovoltaic systems and a precise articulation of their conceptual boundaries. We underscore a shift from structure-oriented material engineering toward biofunction-enabled energy conversion—a transition that enables breakthroughs in power output, system durability, and environmental adaptability. Through systematic comparisons of mechanisms, biomaterial sources, performance metrics, and emerging application scenarios, we identify current bottlenecks and propose targeted strategies. In light of recent trends, living hydrovoltaic systems hold particular promise as a forward-looking direction, offering a transformative platform for future hydrovoltaic internet, intelligence, and ecological integration at scale.
Phototrophy and chemotrophy are two dominant types of microbial metabolism. However, to date, the potential of the ubiquitous and versatile mechanical energy as a renewable energy source to drive the growth of microorganisms has remained unknown and not utilized. Here, we present evidence in favor of a previously unidentified metabolic pathway, in which the electronic energy produced from mechanical energy by the piezoelectric materials is used to support the growth of microorganisms. When electroactive microorganism Rhodopseudomonas palustris (R. palustris; with barium titanate nanoparticles) was mechanically stirred, a powerful biohybrid piezoelectric effect (BPE) enabled sustainable carbon fixation coupled with nitrate reduction. Transcriptomic analyses demonstrated that mechanical stirring of the bacteria–barium titanate biohybrid led to upregulation of genes encoding functions involved in electron and energy transfer in R. palustris. Studies with other electroactive microorganisms suggested that the ability of microbes to utilize BPE may be a common phenomenon in the microbial world. Taken together, these findings imply a long-neglected and potentially important microbial metabolic pathway, with potential importance to microbial survival in the energy-limited environments.
Electron donors are the central drivers of microbial biodegradation, yet conventional sources-derived from light (photoelectrons), electrodes (bias-injected electrons), or chemical substrates (valence electrons)-are scarce in oligotrophic or lightless environments, limiting their environmental applicability. Here, we report the first microbial biofilm-based hydrovoltaic system (mBio-HS) that harnesses the hydrovoltaic effect of water evaporation to provide a sustainable electron source for pollutant degradation. The mBio-HS, constructed simply with electroactive microorganisms, continuously generates a stable electron flow (∼20 μA, ∼0.3 V) solely through the hydrovoltaic effect, without any external energy input. These water-evaporation-induced hydrovoltaic electrons (WEH-e) perform dual functions: sustaining microbial metabolism to form a self-sufficient community and directly reducing organic pollutants. Using methyl orange (MO) as a model azo dye, the system achieved efficient azo-bond cleavage and 90% decolorization within 72 h. This work not only presents the first prototype of a simple biofilm-based hydrovoltaic pollutant-degradation system, but also establishes a mechanistic foundation for harnessing the ubiquitous hydrovoltaic effect in microbial biofilms to power redox reactions-offering a practical route toward zero-energy, environmentally adaptive bioremediation.
The biophotoelectrochemical (BPEC) process offers a controllable and flexible platform for CO2 conversion into hydrocarbon fuels by integrating the functional components of photoelectrocatalysis with biocatalysis. However, the conventional BPEC methanogenesis process often suffers from low efficiency due to the complex and energy-intensive nature of the multiple electron and proton transfer, as well as poor electronic communication at the abiotic-biotic interface. In this study, we present a BPEC system that integrates a natural dual-absorber photoanode, composed of photosystem II and anthocyanin, with a nanobiohybrid photocathode consisting of Methanosarcina barkeri-cyanamide-functionalized polymeric carbon nitride. This system enables complementary panchromatic solar light absorption at the photoanode, while the nanobiohybrids at the photocathode exhibit excellent photosensitivity and strong capacitive behavior, facilitating robust interfacial electronic communication and promoting biocatalytic reactivity. As a result, the system demonstrates superior BPEC methanogenesis over five successive cycles, achieving a high CH4 selectivity (>95 %) under light illumination, both with and without bias assistance. Further research highlights the promising potential of this BPEC system for simultaneously driving methanogenesis and water sterilization. Our findings offer a novel approach to enhancing the multifunctionality of the BPEC system with solar energy, especially in resource-constrained environments.
Filamentous cable bacteria are capable of centimeter-scale long-distance electron transport and play crucial roles in the biogeochemistry of aquatic sediments. However, the mechanisms underlying long-distance electron transport remain incompletely understood. This study reports dynamic contacts between separate filaments of cable bacteria, enabling them to relay electrons between sulfidic and oxic zones. Video microscopy of motile filaments in a microchamber slide setup revealed that some filaments did not fully bridge the gap between the sulfidic and oxic zone, but made transient contact with each other. Contacts were always end-to-end and often occurred repeatedly, in which filaments always followed the same trajectory back and forth. The contact frequency gradually increased over the first 20 days, and then declined afterwards. About 5.5% of cable bacterium filaments were observed to engage in contact events during a 2-hour observation window on day 20. Confocal microscopy confirmed the presence of extracellular polymer substance trails between filaments, which appear to guide consecutive end-to-end contacts. In situ Raman spectroscopy showed that connections enabled redox continuity between reduced and oxidized filaments, thus suggesting inter-filament electron transfer during physical contact. This inter-filament electron transport represents a novel type of microbial cooperation, and appears to be a strategy for establishing optimal connections between spatially separated electron donors and acceptors in a dynamic sedimentary environment.
It has been previously shown that devices based on microbial biofilms can generate hydrovoltaic energy from water evaporation. However, the potential of hydrovoltaic energy as an energy source for microbial growth has remained unexplored. Here, we show that the electroautotrophic bacterium Rhodopseudomonas palustris can directly utilize evaporation-induced hydrovoltaic electrons for growth within biofilms through extracellular electron uptake, with a strong reliance on carbon fixation coupled with nitrate reduction. We obtained similar results with two other electroautotrophic bacterial species. Although the energy conversion efficiency for microbial growth based on hydrovoltaic energy is low compared to other processes such as photosynthesis, we hypothesize that hydrovoltaic energy may potentially contribute to microbial survival and growth in energy-limited environments, given the ubiquity of microbial biofilms and water evaporation conditions.
Ubiquitous non-Fenton-type reactive oxygen species drive abiotic CH4 production, as reported by Shungui Zhou, Yujie Xiong and co-workers in their Research Article (e202403884). This discovery not only significantly broadens our understanding of CH4 production in complex natural environments, but also offers an innovative, simple and sustainable approach for engineering CH4 production as a high-value energy resource.
Abiotic CH4 production driven by Fenton-type reactive oxygen species (ROS) has been confirmed to be an indispensable component of the atmospheric CH4 budget. While the chemical reactions independent of Fenton chemistry to ROS are ubiquitous in nature, it remains unknown whether the produced ROS can drive abiotic CH4 production. Here, we first demonstrated the abiotic CH4 production at the soil-water interface under illumination. Leveraging this finding, polymeric carbon nitrides (CNx) as a typical analogue of natural geobattery material and dimethyl sulfoxide (DMSO) as a natural methyl donor were used to unravel the underlying mechanisms. We revealed that the ROS, photocatalytically produced by CNx, can oxidize DMSO into CH4 with a high selectivity of 91.5 %. Such an abiotic CH4 production process was further expanded to various non-Fenton-type reaction systems, such as electrocatalysis, pyrocatalysis and sonocatalysis. This work provides insights into the geochemical cycle of abiotic CH4, and offers a new route to CH4 production via integrated energy development.
Accumulating evidences are challenging the paradigm that methane in surface water primarily stems from the anaerobic transformation of organic matters. Yet, the contribution of oxygenic photosynthetic bacteria, a dominant species in surface water, to methane production remains unclear. Here we show methanogenesis triggered by the interaction between oxygenic photosynthetic bacteria and anaerobic methanogenic archaea. By introducing cyanobacterium Synechocystis PCC6803 and methanogenic archaea Methanosarcina barkeri with the redox cycling of iron, CH4 production was induced in coculture biofilms through both syntrophic methanogenesis (under anoxic conditions in darkness) and abiotic methanogenesis (under oxic conditions in illumination) during the periodic dark-light cycles. We have further demonstrated CH4 production by other model oxygenic photosynthetic bacteria from various phyla, in conjunction with different anaerobic methanogenic archaea exhibiting diverse energy conservation modes, as well as various common Fe-species. These findings have revealed an unexpected link between oxygenic photosynthesis and methanogenesis and would advance our understanding of photosynthetic bacteria's ecological role in the global CH4 cycle. Such light-driven methanogenesis may be widely present in nature.
Abiotic CH 4 production driven by Fenton-type reactive oxygen species (ROS) has been confirmed to be an indispensable component of the atmospheric CH 4 budget. While the chemical reactions independent of Fenton chemistry to ROS are ubiquitous in nature, it remains unknown whether the produced ROS can drive abiotic CH 4 production. Here, we first demonstrated the abiotic CH 4 production at the soil-water interface under illumination. Leveraging this finding, polymeric carbon nitrides (CN x ) as a typical analogue of natural geobattery material and dimethyl sulfoxide (DMSO) as a natural methyl donor were used to unravel the underlying mechanisms. We revealed that the ROS, photocatalytically produced by CN x , can oxidize DMSO into CH 4 with a high selectivity of 91.5 %. Such an abiotic CH 4 production process was further expanded to various non-Fenton-type reaction systems, such as electrocatalysis, pyrocatalysis and sonocatalysis. This work provides insights into the geochemical cycle of abiotic CH 4 , and offers a new route to CH 4 production via integrated energy development.
Bio-nano hybrids (BNH), combining semiconductors and microorganisms, have shown great promise for effective solar-to-fuel energy conversion. However, the high-energy ultraviolet (UV) photons in the solar spectrum can cause severe photocorrosion of semiconductors and irreversible photodamage to microorganisms within BNH. Here, we developed an encapsulation strategy using natural luminogens with aggregation-induced emission characteristics (AIEgens) to construct a protective layer for BNH, effectively shielding them against high-energy UV photons. We incorporated natural berberine (BBR) into the BNH composed of Methanosarcina barkeri and polymeric carbon nitrides (CNx). The self-assembled BNH-BBR system displayed a 2.75-fold higher CH4 yield than BNH under simulated solar irradiation. Mechanism analysis revealed that BBR acted as a UV sunscreen for BNH by converting high-energy short wavelengths into low-energy long wavelengths, thereby reducing the accumulation of reactive oxygen species and alleviating the photocorrosion of CNx. Furthermore, BBR functioned as a photosynergist for BNH by regulating photoelectron production and utilization, enhancing the intracellular energy formation in M. barkeri for growth and metabolism. This work provides important insights into the effective and scalable conversion of CO2 into valuable biofuels with BNH under light illumination containing high-energy photons.