Novel energy utilization mechanisms of microorganisms in the hydrosphere

Abstract

This review focuses on new approaches adopted by microorganisms to acquire energy in oligotrophic and low-energy hydrosphere habitats, which involves increasing income, reducing expenditure and cooperation among different microorganisms. The various energy sources, electron transfer pathways and carbon, nitrogen, and sulfur cycles are involved in these processes. Specifically, this review delves into the potential molecular mechanisms on microbes utilizing photoelectrons from semiconducting minerals in natural photocatalytic systems. Also, it aims to reveal the regulation mechanisms of photoelectrons on interspecific electron transfer pathways and the energy synthesis processes in Geobacter, Pseudomonas, Halomonas and sulfate reducing bacteria, as well as the molecular mechanisms of perception and adaptation to different potentials of extracellular receptors and changes of oxygen gradients. Moreover, it demonstrates the network structure, formation and mechanisms of long-distance electron transfer driven by cable bacteria, particularly in the context of reducing CH₄ and N₂O coupled with the increase of dimethyl sulfide. This paper attempts to put forward new ideas for the energy utilization by microorganisms and their impact on element cycle in the hydrosphere, which contributes to a better understanding of the energy metabolism in interspecific, interspecies, and ecosystem contexts during the cycle-coupled processes of elements.

1. Introduction

In oligotrophic and low-energy environments that are prevalent in hydrosphere habitats, many microorganisms exhibit the ability to acquire external energy or improve energy conversion efficiency through electron transfer to/from extracellular minerals or other microorganisms. This adaptive strategy allows them to survive in low-energy environments. Numerous studies have reported that microorganisms can efficiently acquire external energy through various electron transfer pathways [1], [2], [3], [4]. For example, some microorganisms can obtain photoelectrons from semiconducting minerals for metabolism [5]. Some microorganisms of different species can establish symbiotic relationships to survive in low-energy environments, for instance, through processes like electron transfer from anaerobic to aerobic microorganisms and direct interspecific electron transfer (DIET) mediated by minerals [6], [7], [8]. In oligotrophic environments, microorganisms can acquire more energy by expanding energy sources, reducing energy consumption, and establishing symbiotic relationships with other microorganisms to cope with the stress of limited energy supply. Unveiling novel electron transfer pathways or energy utilization mechanisms by microorganisms from environmental components is crucial for understanding the survival mechanisms of microorganisms in oligotrophic aquatic environments.

Many attempts have been made to explore how microorganisms utilize novel energy sources to drive biogeochemical cycles of carbon, nitrogen, and sulfur in the hydrosphere. For example, non-photosynthetic and electroactive microorganisms have been found to utilize photoelectrons from semiconducting minerals for growth and metabolism, thereby enhancing the microbial-driven cycling of elements [9], [10], [11]. In addition, it has been found that the relationship between the molecular mechanism of cellular sensing and adaptation to potential gradient [12] and how microorganisms use the network structure of LDET to drive carbon, nitrogen and sulfur cycle and its formation mechanism in the hydrosphere [13], [14].

This review summarizes recent advances in different novel ways of energy uptake by microorganisms in the hydrosphere and the impacts on aquatic ecosystems, specifically including: (a) the impacts of photoelectron utilization on microbial metabolism and the evolution of microbial communities in the euphotic zone; (b) molecular mechanisms and influencing factors for the transmembrane transfer pathways of photoelectrons from extracellular semiconducting minerals to intracellular redox active substances; (c) the regulation mechanism of photoelectrons from various semiconducting minerals on the electron transfer pathway and energy synthesis of Geobacter, Pseudomonas, Halomonas and sulfate-reducing bacteria (Desulfovibrio); (d) the role of a new solar-stimulated energy conversion pathway involving semiconducting iron/manganese minerals and non-photosynthetic microorganisms in driving the cycle of carbon, nitrogen, sulfur and other nutrients in the hydrosphere; (e) the potential pathways or components of Geobacter sulfurreducens (G. sulfurreducens) for sensing changes in redox potentials and initiating the process of “sensing → transferring → responding” in response to potential alternations; (f) molecular mechanism of extracellular electron transfer (EET) and adaptation to oxygen gradient in methane-oxidizing bacteria, along with the interspecific energy cooperation mechanism and methane emission reduction; (g) the structure and formation of the LDET network primarily composed of cable bacteria, and its role in the cycling of elements. This paper reviewed the energy utilization mechanism and carbon, nitrogen and sulfur cycle in the hydrosphere, as well as the scientific support for the conservation and utilization of microbial ecological functions in the hydrosphere. Significantly, it can enhance our comprehension of the interaction and co-evolution between life and global environment.

2. Energy acquisition strategies of aquatic microorganisms

2.1. New energy sources for microorganisms in the hydrosphere

2.1.1. A new way for microorganisms mediated by minerals to capture solar energy

In nature, semiconducting minerals can be excited by solar photons, resulting in the transition of electrons from the valence band to the conduction band, as well as the formation of photo-holes and photoelectrons [15], [16]. Semiconducting minerals with visible light responsiveness are widely distributed in the euphotic zone of offshore and estuary. The highly active photoelectrons generated by these semiconducting minerals under sunlight can function as an important energy source at the Earth's surface, complementing solar photons and valence electrons [5]. This novel energy source might promote the microbially driven cycling of carbon, nitrogen, and sulfur in the euphotic zone of the hydrosphere. Under light irradiation, semiconducting minerals, like goethite, rutile, and sphalerite, have been reported to generate photoelectrons, effectively supporting the growth of chemoautotrophic Acidithiobacillus ferrooxidans, heterotrophic Alcaligenes faecalis, and influencing the structure of microbial communities in natural soils [9,17].

2.1.2. New mechanisms of interspecies electron transfer and energy metabolism

A notable disparity exists in the minimum energy threshold by microorganisms in complex aquatic environments and under the controlled conditions of pure culture systems in the laboratory. This discrepancy is primarily attributed to the capacity of microorganisms in natural environments, belonging to diverse metabolic categories, to maximize energy utilization by establishing syntrophic relationships. Especially in oligotrophic and low-energy aquatic habitats, microorganisms of different species, driven by energy constraints, are compelled to fully harness free energy released during catabolic reactions. Through diverse forms of close cooperation, these microorganisms form a syntrophic relationship with low energy demand and thus become the dominant species in the community. This syntrophic relationship can be achieved through traditional trophic interaction or DIET. Different from trophic interaction, DIET is independent of the formation, accumulation, and diffusion of molecular metabolites, so it can efficiently promote the establishment of syntrophic relationships between different microorganisms. The interspecific electron transfer by different microorganisms can be achieved through direct contact, nanowires, extracellular secretions, and conductive minerals. Through the implementation of a more rational gene mutation strategy, it has been verified that cytochrome c, rather than the nanowires, plays a central role in mediating the transfer of electrons between different species of Geobacter. This clarification rectifies a long-term misunderstanding of the DIET mechanism in Geobacter [6].

2.1.3. A new approach for microbial long-distance electron transfer

The diversity and heterogeneity of environmental conditions in sediments restrict the spatial and temporal distribution, community structure, and metabolic pathways of most microorganisms. However, certain electroactive microorganisms have evolved ways to overcome these limitations by engaging in long-distance electron transfer (LDET) through nanowires, environmental components (such as minerals), or even other microorganisms. This enables the formation of an interspecies-connected electron transfer network and promotes the biogeochemical cycling of elements. Currently, various filamentous bacteria have demonstrated their capacities in facilitating LDET and constructing electron transfer networks. For instance, a type of filamentous Gram-positive bacterium, Lysinibacillus varians GY32 (L. varians GY32), isolated from stream sediments, has been found to elongate cells during electricity generation, resulting in individual cell lengths exceeding 1 mm. This process leads to the formation of a centimeter-scale conductive network. Despite the insulating nature of the cell wall of L. varians GY32 in this conductive network, the pivotal components of this network are the conductive protein nanowires, which span throughout the cells with a length of ten microns [18]. Additionally, the increased concentration of dissolved oxygen in overlying water has been found to significantly improve the abundance of cable bacteria and promote the electrogenic sulfur oxidation process in sediments. This increased abundance of cable bacteria also stimulates the growth of sulfur metabolism-related, organic matter degradation-related, and other electroactive microorganisms, collectively forming a resilient syntrophic network that includes cable bacteria.

2.2. New insights into microbial energy metabolism for driving element cycle

2.2.1. Photoelectrons from semiconducting minerals as an energy source for microorganisms to drive element cycle

Within a complex system consisted of semiconducting minerals and microorganisms under sunlight, mineral photoelectrons have been demonstrated to enhance the growth of non-photosynthetic microorganisms [9], promote carbon sequestration [19], and significantly improve the nitrate reduction efficiency of Halomonas (a model microorganism in nitrogen metabolism) [20]. Elemental sulfur on the surface of sediments in terrestrial hot springs can selectively absorb shortwave ultraviolet light to generate high-energy photoelectrons and induce the formation of sulfur-containing free radicals. This process leads to the reduction of CO₂ and the formation of formic acid, which provides a carbon source for the growth and metabolism of heterotrophic microorganisms in hot springs. It reveals a novel energy source for microorganisms in extreme environments [21]. In addition, the energy of highly active photo-holes produced by semiconducting minerals under sunlight irradiation may also promote the metabolism of non-photosynthetic microorganisms. It has been found that Shewanella oneidensis MR-1 (S. oneidensis MR-1) generates electrons from lactate metabolism and utilizes them to fill photoexcited holes in hematite under simulated sunlight. The generated photoelectrons from hematite can effectively reduce Cr(VI), resulting in the enhanced reduction efficiency of Cr(VI) and the tolerance of S. oneidensis MR-1 to Cr [10]. This study illustrates how electroactive microorganisms and semiconducting minerals can synergistically convert light energy and drive the element cycle [10]. Thus, these studies have shown that both photoelectrons and photo-holes from semiconducting minerals can enhance microbial metabolism, thereby facilitating the microbial-driven carbon, nitrogen, and sulfur cycles in the hydrosphere.

2.2.2. Interspecies electron transfer mediated by minerals for driving element cycle

The discovery of a new approach for bacteria to engage in interspecies electron transfer using electron mediators such as flavin, vesicles, and conductive iron oxide minerals [22], [23] deepens our understanding of the diversity in the pathways of interspecies electron transfer. It has been revealed that the functions and distribution of hydroquinone oxidase and quinone reductase on the plasma membrane of microbial cells are specific, exerting a regulatory effect on the EET process of microorganisms. These findings contribute to a comprehensive understanding of the pathway of mineral-mediated interspecies electron transfer [24]. Consequently, investigating the intricate and diverse processes of interspecies electron transfer in the hydrosphere is critical for understanding the unresolved biogeochemical element cycles in complex aquatic habitats. It can also shed light on the correlation between key functional microorganisms and microbial communities in the process of energy metabolism.

2.2.3. LDET for driving element cycle in microbial electron transfer networks

The robust syntrophic network involving cable bacteria accelerates the transformation of refractory organic carbon and affects the key ecological processes in the carbon and sulfur cycle in subsurface sediments. A proposed extension mechanism of electric oxygen mediated by cable bacteria offers a novel perspective for understanding these biogeochemical and ecological processes [13]. The following study has further demonstrated that the addition of electrodes to sulfide-rich sediments significantly enhances the EET activity of microorganisms. The electrons from electrodes facilitate the enrichment of various filamentous microorganisms with sulfur redox capacities around the electrodes, triggering the formation of a microbial network that can extend several centimeters. This network accelerates sulfide oxidation in deep sediments [25]. Collectively, these results reveal a novel mechanism by which microorganisms regulate biogeochemical cycles in the hydrosphere, highlight the immense potential of microbial LDET networks in driving the element cycle, and expand our understanding of the physiological and ecological functions of electroactive microorganisms.

2.3. Current research and progress in energy metabolism pathways of aquatic microorganisms

Some progress has been made in revealing the new energy metabolism mechanisms of aquatic microorganisms, including the uptake of mineral photoelectrons, the establishment of syntrophic relationships, and the utilization of microbial LDET networks (Fig. 1).

Fig. 1.

Current research and progress of energy metabolism pathways of microorganisms in the hydrosphere. (a) The conversion of solar energy by semiconducting minerals provides a new energy source for microbial energy metabolism and carbon sequestration in the euphotic zone. (b) Long-distance electron transfer (LDET) networks extend the distance of microbial electron transport from micrometers to centimeters, overcoming spatial isolation of redox processes and niche constraints. (c) Trophic interaction and symbiotic relationship established through direct interspecies electron transfer overcome the energy barrier and maximize energy utilization.

These novel energy utilization methods contribute to the survival of microorganisms in oligotrophic environments with low-energy supply, which are widespread in the hydrosphere habitats. To cope with energy limitation, microorganisms have developed various strategies for efficiently acquiring and utilizing energy to drive the carbon, nitrogen, and sulfur cycles in oligotrophic environments. These strategies include: improving energy conversion efficiency (reducing expenditure), and establishing trophic interaction and syntrophic relationship (cooperation). (1) “Increasing income”, i.e. acquiring more energy by utilizing different forms of external energy. Non-photosynthetic microorganisms in the euphotic zone utilize solar energy through the light-to-electron conversion mediated by semiconducting minerals. Previous research has confirmed that mineral photoelectrons play an important role in regulating EET of microorganisms and driving biogeochemical cycles of elements [11,[26], [27]]. The utilization of mineral photoelectrons expands the types of energy sources for non-photosynthetic microorganisms [19]. (2) “Reducing expenditure”: the function of LDET enables cable bacteria to connect the aerobic and anaerobic zones to transfer electrons. This capability helps aquatic microorganisms to overcome the restriction of low-concentration oxygen on microbial metabolism and drives the coupling of oxygen reduction with the cycles of carbon, sulfur, and other key elements in heterogeneous sediments. Such LDET-based energy utilization represents a new mechanism how microorganisms obtain enough energy to drive elemental cycling in oligotrophic sediments. It also provides a new perspective for a deeper understanding of the structure, formation, and mechanism of microbial LDET networks. (3) Cooperation: microorganisms with different metabolic pathways can establish syntrophic relationships through DIET to adapt to oligotrophic and low-energy aquatic habitats and drive the carbon, nitrogen, and sulfur cycles. Collectively, these advancements reflect the diversity and uniqueness of microbial metabolic pathways, energy acquisition, and storage modes in aquatic environments, especially in the oligotrophic and low-energy aquatic habitats.

3. Novel ways of energy uptake by microorganisms in the hydrosphere

3.1. Natural photocatalysts for supplying photoelectrons as an energy source to microorganisms in euphotic zone

Semiconducting minerals can convert solar photons into high-energy photoelectrons under solar excitation and therefore act as natural photocatalysts in the euphotic zone [5]. The photoelectrons generated by semiconducting minerals can directly interplay with non-photosynthetic microorganisms [9,[28], [29]]. Under light irradiation, photoelectrons from a semiconductor CdS can be transported to intracellular redox compounds of non-photosynthetic microorganisms via transmembrane electron transfer pathways, promoting cell metabolism and CO₂ fixation [19,[30], [31]]. Recent studies reveal a significant presence of suspended semiconducting mineral particles from terrestrial or secondary sources, such as goethite, hematite, birnessite, rutile, anatase, and brookite, exhibiting excellent photocatalytic activities in the euphotic zone of estuarine and offshore environments [11,27,32]. The system of marine-sunlight-semiconducting minerals has a significant photocatalytic effect to form the natural photocatalytic system of the hydrosphere euphotic zone (Fig. 1), which plays an important role in geochemical element cycle and energy flow in the critical zones.

Some transcriptomic and proteomic studies have showed that photoelectrons may transported through cell membranes of non-photosynthetic microorganisms to promote microbial growth and metabolism and affecting the transformation of organic substances in the environment [30], [31]. Liu et al. [32]. applied gene knockout techniques to demonstrate that the photoelectrons produced by anatase, a typical semiconducting mineral in the hydrosphere euphotic zone, can facilitate the growth and metabolism of the electroactive bacterium Pseudomonas aeruginosa PAO1 (P. aeruginosa PAO1) and enhance the EET process. The results indicated that extracellular polymeric substances (EPS) are the key components involved in the transfer of photoelectrons between anatase and P. aeruginosa PAO1. It has been demonstrated that the photocatalysis of goethite, a typical semiconducting mineral in the euphotic zone, can regulate the structure and function of the microbial community in the hydrosphere by affecting microbial growth and metabolism using mineral photoelectrons [11]. Besides, the photoelectrons generated by CdS can facilitate the fixation of carbon dioxide by non-photosynthetic autotrophic Moorella thermoacetica and genetically engineered Saccharomyces cerevisiae [33], [34]. Additionally, Denitrifiers can also use photoelectrons of semiconducting minerals for nitrate reduction. For example, CdS can collaboratively promote the reduction of NO₃⁻ to N₂O by Thiobacillus denitriicans under light irradiation. The photoelectrons generated by CdS can be transferred to cells to the enzymes in the denitrification pathway through the transmembrane electron transfer chain [35]. Notably, there is a discovery that Halomonas sp. strain 3727 isolated from the marine euphotic zone has the ability of denitrification, which can reduce nitrate to ammonium. It was indicated that the microbial community evolution can change significantly under simulated photoelectrons with different energies. The stable isotope technique was applied to trace the existing state and transformation process of elements regulated by electroactive microorganisms. It was suggested that semiconducting mineral photoelectrons play a vital role in the nitrogen element cycle mediated by microorganisms offshore [20,36]. Under light conditions, the photoelectrons from elemental sulfur can reduce carbon dioxide to small organic molecules, such as formic acid [21], which may be used by marine heterotrophic microorganisms for synthesizing biomass, thus indirectly affecting microbial metabolism and energy conversion. Correspondingly, semiconducting minerals can also produce photo-holes that have high activities to oxidize and decompose complex macromolecules, resulting in small organic molecules that can be utilized by microorganisms in marine environments [24]. These findings revealed the potential impacts of semiconducting photoelectrons on the biogeochemical element cycle in the euphotic zone.

With solar radiation, microbial ecosystems worldwide serve as the support system of the biosphere and profoundly affect the hydrosphere, lithosphere, and atmosphere. Microbial ecosystems play a key role in regulating the global material and energy cycle, actively participating in driving the biogeochemical carbon, nitrogen, and sulfur elements cycle [37], [38], [39]. The unique photocatalytic activity of semiconducting minerals enables them to capture and convert solar energy to generate photoelectrons with high activities, which might promote the growth and metabolism of microorganisms and affect the cycling of carbon, nitrogen, sulfur, and other nutrient elements in the euphotic zone (Fig. 2). It's important to deepen our understanding of how microorganisms utilize various energy sources, including photoelectrons from natural photocatalytic systems, for metabolism and to discern the contributions of these energy sources to microbial ecosystems [40].

Fig. 2.

Production and transfer of mineral photoelectrons and energy metabolism of microorganisms.

3.2. Visible light stimulated synergy between semiconducting iron minerals and non-phototrophic microorganisms for nutrient element cycle

Active photoelectrons and photo-holes can react with a variety of organic pollutants, redox-active ions, and electroactive microorganisms in natural environments. In particular, the photoelectrons generated by semiconducting minerals can be an energy source for non-photosynthetic microorganisms that possess the ability of EET. Semiconductor-microorganism hybrid systems under sunlight irradiation have been proposed as a versatile platform for solar-to-chemical production or solar-to-electricity conversion. However, the molecular mechanism underlying the uptake of photoelectrons by microorganisms for energy or biomass production remains elusive. Further studies are needed to investigate whether photoelectrons derived from naturally occurring semiconductors can substantially contribute to the metabolism of electroactive microorganisms within complex environments, where various redox-active components may compete for these photoelectrons. Recent studies showed that electroactive microorganisms, such as S. oneidensis MR-1, can use the photogenerated holes produced by semiconducting minerals under sunlight irradiation as terminal electron acceptors. In anaerobic or microaerobic environments, S. oneidensis MR-1 typically couples the oxidation of organic substrates with the bioreduction of minerals containing high-valence metal ions, such as Fe(III) or Mn(IV), through EET pathways. As a result, reduced metal ions are released from the minerals, leading to reductive dissolution and/or transformation of the minerals. When S. oneidensis MR-1 transfers electrons to fill the photo-holes of semiconducting minerals, like hematite, in sunlight, the photoelectrons in the minerals can be efficiently separated from the photo-holes, enabling them to react with nutrient elements or heavy metals in the surrounding environments. Moreover, as photocatalysts, semiconducting minerals remain unchanged throughout the process. The mechanism of the light-triggered electron transfer pathway between semiconducting minerals and electroactive microorganisms has been investigated by Qian et al. [41]. using a solar-assisted microbial photoelectrochemical system (solar MPS) with a hematite nanowire photoelectrode covered by a biofilm of S. oneidensis MR-1 under sunlight irradiation. It was found that the photocurrent intensity under light conditions was 2.5 times higher than that in dark. When S. oneidensis MR-1 was deactivated, the photocurrent was decreased significantly, indicating that living cells, rather than EPS, are critical for the light-to-electricity conversion in the photocatalyst-electricigen hybrid system [41]. Furthermore, Zhu et al. [42]. investigated how the supply rates of bio-electrons by electroactive microorganisms affect photocurrents in the solar MPS with wild-type and bio-engineered S. oneidensis MR-1, respectively. To accelerate lactate oxidation and the supply rate of bio-electrons, the d-lactate transporter gene, SO1522, was overexpressed in the bio-engineered S. oneidensis MR-1. The generation efficiency of photocurrents in the system with genetically engineered S. oneidensis MR-1 is 36% higher than that with wild- type under otherwise identical conditions, suggesting that the metabolism rates of electrogenic microorganisms, and consequently their supply rates of bio-electrons, have a substantial influence on the efficiency of the light-to-electricity in the hybrid system with hematite and S. oneidensis MR-1 under sunlight [42].

The sunlight-triggered electron transfer pathway not only promotes the light-to-electricity conversion but also enhances the microbially-mediated transformation of nutrient elements and heavy metals. For example, the study on the bio-reduction of Cr(VI) by S. oneidensis MR-1 and hematite has revealed that sunlight can trigger an additional electron transfer pathway: lactate→ S. oneidensis MR-1→ hematite→ Cr(VI), leading to a substantial enhancement in Cr(VI) removal and microbial metabolism [10] (Fig. 3). The results have indicated that S. oneidensis MR-1 is capable of enzymatically reducing Cr(VI) while concurrently transferring bio-electrons to fill the photo-holes of hematite within the batch reactor, all without the need for an external electric field. Furthermore, the bio-electrons from S. oneidensis MR-1 effectively occupy the photoexcited holes in hematite, thereby impeding the recombination of photoexcited charge carriers and, consequently, promoting the reduction of Cr(VI) by hematite photoelectrons. In addition, the reduction of Cr(VI) by hematite photoelectrons accelerates the precipitation of Cr(III) on the mineral surface and therefore reduces the toxicity of Cr(VI) or/and Cr(III)-containing reduction products to the cells. The study also shows that, under light irradiation, organic hole scavengers, like ethylenediaminetetraacetic acid (EDTA), can further boost the removal of Cr(VI) by hematite and S. oneidensis MR-1. This is because EDTA and bio-electrons from S. oneidensis MR-1 can simultaneously fill photo-holes, thus enhancing the efficiency of hematite photoelectrons in reducing Cr(VI). The findings suggest that, in natural environments with various photo-hole scavengers, the light-triggered synergy of semiconducting minerals and electrogenic microorganisms still can contribute substantially to the conversion of solar energy to reducing power for the immobilization of heavy metals and the reduction of nutrient elements.

Fig. 3.

A new mechanism of visible light stimulated synergy between iron oxide semiconducting minerals and electroactive microorganisms for driving Cr(VI) reduction[10].

In addition to the system involving the model electroactive microorganisms S. oneidensis MR-1 and hematite, this collaborative conversion of light energy by semiconducting minerals and electrogenic microorganisms is also observed in various microbe-mineral systems [26,43]. For example, it was found that the removal extent of nitrate by hematite and P. aeruginosa PAO1 under light irradiation reached 90.49% ± 4.40% within 2.5 h, which was 1.3 times higher than that in the dark and 1.43 times greater than that of the system without minerals. Electrochemical impedance spectroscopic spectra revealed a notable decrease in the internal charge transfer resistance within the system consisted of hematite and P. aeruginosa PAO1 after exposure to sunlight. When hematite was replaced with natural red soils, it was found that the removal extent of nitrate could reach 80.56% within 2.5 h under sunlight. The findings demonstrated that the biogeochemical cycle of nitrogen can be affected by the light-induced synergy between semiconducting minerals and heterotrophic denitrification microorganisms. This phenomenon may be widespread in topsoils [44]. In the hematite-Lactococcus lactis system, the consumption rate of glucose and the efficiency of electron transfer were markedly increased by sunlight irradiation, when compared to the values in the dark. In the system with red soil and Lactococcus lactis, exposure to sunlight irradiation led to a glucose consumption rate that was 2.5 times higher than the value observed in the absence of light. Thus, the widespread semiconducting minerals at Earth's surface have the potential to greatly enhance the microbial conversion of organic compounds when exposed to sunlight [45].

The aforementioned studies have revealed a novel mechanism illustrating how semiconducting minerals and microorganisms collaborate to convert light energy to reduction power in the euphotic zone. This mechanism could play an important role in various biogeochemical processes, such as the immobilization of heavy metals and the cycling of nutrients, like carbon, nitrogen, and sulfur. It offers a new perspective on understanding microbial-driven element cycles in the hydrosphere, sparking interest in synthetic biology, environmental remediation, and renewable energy.

3.3. Potential sensing pathway for extracellular receptors adaptation in G. sulfurreducens

Respiring extracellular electron acceptors is the dominant energy generation way of anaerobic microorganisms in some anaerobic environments. However, those electron acceptors usually have different redox potentials, and it is necessary for those microorganisms to evolve some sophisticated mechanisms to adapt the variable redox conditions. Geobacter is the typical anaerobe proficient in reducing and utilizing prevalent electron acceptors across various oxidation states in aquatic environments and thus it is an important driver in the biogeochemical cycle of Fe/C/N/S. The ability of Geobacter to harness various electron acceptors with a broad range of potentials makes it a predominant bacterial group in the extracellular respiratory environment, occupying a significant ecological niche. The essence of Geobacter’s extracellular respiration lies in utilizing the potential difference created by the oxidation of electron acceptors and the reduction of electron donors to facilitate EET and generate energy. Geobacter possesses different EET pathways to realize the effective utilization of different receptors. Levar et al. [46]. proposed that G. sulfurreducens can, at least, achieve the reduction of high/low potential receptors by expressing three intima quinone oxidoreductases (CbcAB, CbcL, and ImcH) [46], [47]. When the receptor redox potential is high (> −0.10 V vs SHE), G. sulfurreducens uses ImcH to transfer electrons from the quinone pool [48]. Conversely, when the receptor potential is low (< −0.10 V), G. sulfurreducens utilizes CbcL to capture electrons in the quinone pool [49]. When the midpoint potential of receptors is less than −0.21 V (approaching the thermodynamic limit of respiration), G. sulfurreducens is likely to exclusively depend on CbcAB to transfer electrons [47]. G. sulfurreducens can also regulate the expression of genes for intracellular energy metabolism and other electron transfer-related proteins to achieve the reduction of different potential receptors [50], [51]. Therefore, we speculate that Geobacter may have the ability to sense receptor potentials and thereafter to regulate extracellular respiration (i.e., there may be a potential sensing pathway) to adapt to different extracellular receptors with distinct potentials.

The identification of a microbial anoxic redox control system (Arc system) provides theoretical implications for understanding Geobacter’s sensing behavior for receptor potentials. The Arc system serves as a mechanism for microorganisms to sense environmental oxygen concentrations and maintain intracellular redox balance by regulating the expression of genes related to cell metabolism [52]. In 1988, Iuchi et al. [53] initially reported the Arc system using Escherichia coli (E. coli) as a model strain. It is a dual-component system composed of a membrane-bound sensor histidine kinase (ArcB) and a response regulatory protein (ArcA). In this system, ArcB indirectly perceives the ambient oxygen concentration by directly sensing the redox state of the intima quinone pool [54]. When E. coli is under anaerobic or anoxic conditions, reduced quinone accumulates, which induces the phosphorylation ArcB and then triggers phosphorely to further phosphorylate ArcA. The phosphorylated ArcA (ArcA-P) inhibits the expression of oxidase at the aerobic cytochrome b₀ terminal but activates the expression of cytochrome b_d terminal oxidase, which has a higher oxygen affinity. These processes help cells to maximize oxygen availability in anoxic environments. On the contrary, when the environment becomes aerobic, ArcB undergoes dephosphorylation and thus exhibit phosphatase activity. This activity can further catalyze ArcA dephosphorylation and remove the transcriptional regulation of ArcA on related genes [55] (Fig. 4A). As a consequence, the Arc system senses the environmental oxygen concentrations by sensing the redox status of the intima quinone pool, thereby regulating cellular function at the subcellular level. It has been demonstrated that electrode potential can also affect the redox state of the intima quinone pool [56]. S. oneidensis MR-1 connects the intima quinone pool to the electrodes through EET pathways and regulates the expression of the catabolic pathway by the Arc system. Different from the typical Arc system, the Arc system of S. oneidensis MR-1 consists of sensor histidine kinase (ArcS), histidine phosphor transfer protein (HptA) and response regulatory protein (ArcA). The ArcS dimer responds to the reduced quinone pool and transfers the phosphate group to ArcA via HptA after completing self-phosphorylation (Fig. 4B).

Fig. 4.

The Arc system and simplified model of phosphate transfer in E. coli (A) and S. oneidensis (B), respectively.

The EET chain of Geobacter can link the oxidation of the intima quinone pool with the reduction of extracellular receptors [1,57]. Given the presence of multiple homologous proteins of the dual-component system in the genome, it can be speculated that Geobacter likely possesses a receptor “potential sensing pathway” dependent on the Arc system. Through this system, the extracellular receptor potential can be related to intima quinone pool redox states. Furthermore, the Arc system will convert the “potential signal” to “cell signal” via phosphate transfer, regulating the expression of extracellular respiration-related genes to adapt to different receptor potentials (Fig. 5).

Fig. 5.

The Arc system of Geobacter.

3.4. Interspecific energy cooperation mechanisms of methane-oxidizing bacteria

Methane-oxidizing bacteria play a pivotal role in reducing methane emission. A strain of methane-oxidizing bacteria isolated from the Yellow River Delta wetlands, identified as Methylobacter, has been found to significantly influence the properties of methane sinks in deltas [58]. However, the mechanism of methane oxidation driven by aerobic methane-oxidizing bacteria in hypoxic or anoxic habitats remains unclear. Also, it has been reported that aerobic methane-oxidizing bacteria in anoxic habitats independently facilitate methane oxidation through fermentation or denitrification, but the mechanism of energy metabolism are yet to be elucidated. Methane-oxidizing bacteria, under hypoxic or anoxic conditions, can release fermentation byproducts, such as formic acid, acetic acid, citric acid, or succinic acid, into the environment [59]. The production of fermentation acids represents a genetic-evolutionary strategy employed by methane-oxidizing bacteria to improve the tolerance of nutrient-deprived cells or adaptability in the hypoxic environments. Typical aerobic methane-oxidizing bacteria, such as Methylobacter or Methylomonas, harbor incomplete denitrification functional genes, enabling them to employ NO₃⁻/NO₂⁻ as electron acceptors for methane oxidation when oxygen is insufficient [60]. Moreover, under conditions of limited oxygen, Methylobacter and Methylotenera exhibited mutual growth interaction, with Methylotenera regulating the functional proteins of Methylobacter to stimulate the secretion of methanol for its own growth [61].

EET and DIET provide a new perspective for exploring methane oxidation in anoxic environments. Notably, the electron interplay between Methanogens and Desulfovibrio, as well as the EET capacity of methane-oxidizing bacteria, has expanded our understanding of electroactive microorganisms [62], [63]. These findings collectively provided a theoretical basis for the interspecific electron transfer and energy-cooperative mechanism of anoxic methane oxidation, primarily driven by aerobic methane-oxidizing bacteria. It has been found that Methylomonas sp. LW13 and Methylosinus sp. LW4 utilize unidentified proteins within the T1SS system as electron shuttles, coupling methane oxidation with the reduction of Fe(III)-bearing minerals in hypoxic conditions [64]. Furthermore, Wang et al. [65] explored that the electricity generation and metal reduction capacities of aerobic methane-oxidizing bacteria are significantly decreased through knocking out epsH genes associated with biofilm formation. This finding highlights the pivotal role of redox activity of biofilms in the electron transfer process [65]. Methylococcus capsulatus (Bath) is another model methanotroph that has the EET ability to reduce ferrihydrite. Unlike Methylomonas sp. LW13, M. capsulatus (Bath) has cytochrome c genes homologous to the β-barrel outer membrane protein gene (mtrB) of S. oneidensis. Furthermore, Tanaka et al. [66] found that the current production of M. capsulatus was significantly suppressed by treatment with carbon monoxide gas, an inhibitor of cytochrome c. This observation provides compelling evidence of EET in M. capsulatus (Bath) and underscores the pivotal role of cytochrome c in this process. On the other hand, aerobic methane-oxidizing bacteria can also interact with other microorganisms through DIET. Shi et al. [67] discovered that Methylocystis can collaborate with Pseudoxanthomonas, leading to the concurrent processes of methane oxidation and selenate reduction in biological sludge reactors, as evidenced by metagenomic data. Besides, Chang et al. [68] identified the presence of sulfate-reducing bacteria, like Desulfovibrio, in a membrane biological sludge reactor, which can be attributed to the occurrence of intermediate formic, acetic acid, or interspecific electron interaction in Methylobacter. Nevertheless, the mechanism of electron transfer and energy metabolism in the aforementioned studies have yet to be elucidated.

Methylobacter, Methylomonas, and other strains of methane-oxidizing bacteria, capable of utilizing non-oxygen electron acceptors under hypoxic conditions, have been selected as model strains for studying the mechanism of interspecific electron transfer [69] (Fig. 6). The EET capability of these methane-oxidizing bacteria has been preliminarily verified using bioelectrochemical systems [64]. Given the EET capability of aerobic methane-oxidizing bacteria, a hypothesis has been posited suggesting that aerobic methane-oxidizing bacteria can mediate EET/DIET to drive anoxic methane oxidation. This implies that the oxidation of methane by aerobic methane-oxidizing bacteria may depend on the transfer of electrons produced from methane oxidation to extracellular electron acceptors, such as iron oxides, humus or electrodes in hypoxic or anoxic conditions. Alternatively, DIET involving microorganisms that can act as extracellular electron acceptors, like sulfate-reducing bacteria, may play a crucial role in sulfate-rich coastal environments.

Fig. 6.

A schematic diagram of soil hypoxic methane oxidation in the Yellow River Delta wetlands[69].

3.5. Structure and mechanism of microbial LDET networks

Electroactive microorganisms are widely distributed in aquatic environments, significantly contributing to the element cycle through EET and the associated electron transfer networks [70], [71], [72]. In recent years, advancements on the mechanism of microbial electron transfer, particularly the identification of filamentous electroactive microorganisms, such as cable bacteria [73] or L. varians GY32 [18], have extended the recognized distance of microbial electron transfer from nanometers to centimeters or even longer distances [71,74]. Taking cable bacteria as an example, they achieve a spatially isolated redox process by mediating long-distance electron transfer with the length of up to 4 cm [73]. An increasing number of studies have indicated that filamentous electroactive microorganisms probably have the capability to form LDET networks through interactions with other functional microorganisms in their surrounding environment, collectively driving the element cycle [13,[75], [76]].

Cable bacteria, a kind of filamentous electroactive microorganisms, were first reported by Lars Peter Nielsen in 2010 [77]. Forming long linear structures by connecting thousands of cells end to end and wrapping them in protective sheathes, cable bacteria exhibit the capability of LDET across different redox environments. These cable bacteria can grow to several centimeters, in length, with densities reaching as high as 117 m·cm⁻³ [73,78]. They facilitate metabolic coupling between different species, which mediates redox processes across different elements [75]. Increasing evidence indicated that cable bacteria play a significant role in sediment acidification and SO₄²⁻ accumulation by coupling spatially isolated redox reactions, a phenomenon known as electrogenic sulfur oxidation [76,79]. Owing to their unique structure and electron transfer mode, cable bacteria have the potential to extend the influence of elevated dissolved oxygen (eDO) in anaerobic sediments. This occurs through the alteration of sediment physiochemical properties and the reinforcement of interspecific interactions with related functional microorganisms [13] (Fig. 7).

Fig. 7.

Conceptual summary of the influence of eDO on sediment biogeochemical processes and interspecific interactions involving cable bacteria and related functional microorganisms[13].

Recently, we found a variety of filamentous electroactive microorganisms in the river sediments of the Pearl River Delta. High-throughput sequencing results showed that some of these microorganisms have high similarity (> 97%, V3-V4 hypervariable regions) with cable bacteria [13], while others, such as L. varians, exhibited low homology (< 85%) with cable bacteria and displayed a remarkably long single-cell length of 1 mm [18]. The distribution of cable bacteria exhibited a distinct biogeographic distribution pattern in the Pearl River Delta, influenced by water quality. High diversity was observed in rivers classified as water quality IV and V rivers [80]. With the proliferation of cable bacteria, the abundance of various functional bacteria (such as sulfur metabolism, organic matter degradation, and electroactive microorganisms, etc.) increased significantly. These microorganisms formed a closely-knit, mutually beneficial syntrophic network with cable bacteria. Notably, L. varians GY32 holds the record as the longest single-cell Gram-positive bacterium documented to date. It is capable of bidirectional EET and can form centimeter-scale conductive microbial networks. The LDET networks of L. varians GY32 consist of filamentous, unicellular cells, and extracellular nanowire-like appendages, representing a combination of the two LDET network modes observed in Gram-negative bacteria, cable bacteria and Geobacter [18] (Fig. 8).

Fig. 8.

Three representative microbial LDET models[18].

A recent discovery highlights that cable bacteria play a regulatory role in the release of the greenhouse gas CH₄ in rice-vegetated soils. This is achieved through their unique LDET function, coupling with relevant functional microorganisms [81]. Nevertheless, research on cable bacteria-long-distance electron transfer networks (CB-LDETNs), particularly their structure and function in regulating the release of greenhouse gases, remains limited.

4. Conclusion

Energy metabolism is the core of microbial life activities, driving the growth and metabolism of microorganisms and the geochemical element cycle in the hydrosphere. Research on microbial metabolism of pure culture systems in the laboratory fails to adequately reflect the methods and strategies for obtaining and metabolizing energy by microorganisms in oligotrophic and low-energy natural habitats. In addition, it also ignores the possibility of functional microorganisms using environmental media or cooperating closely with different microorganisms to make maximum use of the free energy released in the electron transfer process with higher energy. Hence, how do microorganisms acquire and reserve energy for growth and metabolism in specific hydrosphere habitats? How do activities of microbial growth and metabolism participate in the hydrosphere and affect energy flow among different spheres of the Earth? What are the relative contributions of typical functional microorganisms driving energy metabolism and transformation processes to the carbon, nitrogen, and sulfur cycle, as well as the formation and evolution of the habitable globe? Therefore, the crucial factor in exploring the mystery of the microbe driving element cycle is to elucidate the approaches of energy capture, storage, and transfer of microbes in the hydrosphere.

The methods and strategies of functional microorganisms with low productivity to obtain and metabolize energy include cooperating with abiotic environmental media, such as using mineral photoelectrons, and cooperation between different microbial species, such as anaerobic to aerobic electron transfer and DIET. Therefore, research on the electron transfer modes and mechanisms between microorganisms and environmental media is helpful to reveal the energy metabolism pathways in the natural hydrosphere environment. According to the research on the new regulation mechanisms of energy conversion and metabolism, there are three new ways of microbial energy metabolism in the hydrosphere. (1) Microorganisms can use photoelectrons generated by semiconducting minerals under photoexcitation as an energy source in the euphotic zone. (2) Cable bacteria can form long linear structures to carry out LDET and overcome the limitation of insufficient electron acceptors in deep sediments. (3) Different species can use minerals for DIET to form syntrophic relationships and improve energy conversion efficiency.

At present, research on microbial energy metabolism mainly focuses on pure culture microorganisms to quantify the energy flow in the process of microbial metabolism with sufficient substrate. Nevertheless, in the complex hydrosphere habitats, there are still limitations in exploring microbial energy metabolism and transformation. (1) The source of energy is single. Most research on the energy metabolism of hydrosphere microorganisms mainly concentrates on valence electrons and solar photons, but there are few mechanisms for the acquisition, utilization, and transformation of other types of energy in hydrosphere habitats. In recent years, with the deepening of extreme life and low-energy life in special habitats such as polar, deep sea, and deep biosphere, new energy metabolism methods without relying on traditional photoenergy or chemoautotrophy have attracted extensive attention. Particularly, mineral photoelectrons may play an important role in driving and regulating the energy metabolism of microbes in the hydrosphere. (2) The influence of environmental heterogeneity is unclear. Spatial heterogeneity of environmental conditions is common in the hydrosphere habitats, leading to diversity in nutrition, energy sources, chemical composition, etc., which is immensely different from the microbial culture systems with sufficient and well-mixed substrates. In the special oligotrophic and low-energy habitats, microorganisms may evolve unique ways to acquire energy and metabolize. However, these special metabolism pathways may not play a leading role in the culture system, resulting in the survival strategy of microorganisms to adapt to oligotrophic or energy-restricted environments is still ambiguous. (3) The mechanism of microbial-environmental media synergistically driving energy conversion is unknown. A large number of hydrosphere microorganisms (such as methanogens, methanotrophs, iron-oxidizing bacteria, etc.) obtain very little energy through valence electrons, and the energy basis that drives large-scale element cycle in aquatic habitats remains a mystery. Hydrosphere microorganisms may be forced by energy constraints, and closely cooperate with abiotic environmental media (such as minerals, and natural organic matter) or different kinds of species, to maximize the free energy released by catabolic reactions. Whereas, the energy coupling mechanism between microorganisms and environmental media and its role in the element cycle remains to be investigated thoroughly.

Obviously, in the oligotrophic and low-energy hydrosphere, it is necessary to systematically explore how hydrosphere microorganisms transfer mineral photoelectrons and valence electrons to interspecific receptors and drive energy synthesis and storage, to thoroughly comprehend how they take advantage of mineral photoelectrons and valence electrons, how to establish syntrophic relationship and how to construct energy transfer network. In the meanwhile, it is essential to analyze how different types of electroactive microorganisms synergistically construct microbial networks in sediments and carry out long-distance energy transmission. Additionally, it is necessary to elucidate the regulatory and influence mechanisms on energy conversion efficiency of the syntrophic relationship between different species. Thus, it can reveal the main strategies to overcome low-energy supply improve energy conversion and utilization efficiency, and establish a new model of microbial energy metabolism in the oligotrophic and low-energy supply hydrosphere (Fig. 9).

Fig. 9.

Key scientific issues of energy conversion and metabolism of aquatic microorganisms in oligotrophic environments.

So far, we have revealed the strategies of hydrosphere microorganisms to adapt to special aquatic habitats, obtain and utilize limited energy, and drive the carbon, nitrogen, and sulfur cycle. Aiming at hydrosphere habitats with oligotrophic and low-energy supply, we intend to further deepen the perception of increasing income, reducing expenditure and cooperation by microbes. In terms of new energy sources, LDET networks, and interspecies electron transfer, especially based on the previous revelation of the new types and ways of microbial energy utilization, this research will focus on the diversity of microbial energy sources and electron transfer modes in the hydrosphere and its relationship with the carbon, nitrogen, and sulfur cycle. Thus, the key scientific problem of new ways and regulation mechanisms of energy conversion and metabolism of microbes in the hydrosphere can be resolved, including the molecular mechanism of mineral photoelectrons ingested and utilized by microorganisms and the ecological role in driving carbon, nitrogen, and sulfur element cycle in the hydrosphere, the molecular mechanisms of cell sensing and adaptation to potential gradients of electroactive microorganisms concerning carbon, nitrogen and sulfur cycle, the structural characteristics and formation mechanism of the microbial LDET network driving greenhouse gas emission reduction. This paper attempts to provide new ideas for understanding the energy uptake mechanisms of microorganisms and their impact on the carbon, nitrogen, and sulfur cycle in the hydrosphere, which is also conducive to comprehending the basis of interspecific energy metabolism, interspecies, and ecosystem during the cycle-coupled process of various elements. What's more, it can reflect the diversity and uniqueness of microorganisms and their metabolic pathways as well as the modes of energy capture and storage in oligotrophic and low-energy aquatic habitats. This research will enrich the perception of the interaction and co-evolution between life and the global environment. Moreover, it will provide scientific support for the protection and utilization of microbial ecological function of driving carbon, nitrogen, and sulfur cycle in the hydrosphere.

5. Outlook

5.1. Characteristics of the natural photocatalytic system and diversity of microbial energy sources and electron transfer modes in the hydrosphere euphotic zone

This research will further explore the characteristics of the natural photocatalytic system composed of iron, manganese, and titanium oxide semiconducting minerals such as hematite, goethite, birnessite, rutile, anatase and brookite in the euphotic zone and the mechanism of photoelectron energy generation to investigate the kinetic characteristics of Fe(II) and Mn(II) and valence electron energy generation in the photoreduction of goethite and birnessite driven by photoelectrons of semiconducting minerals. Besides, the regulatory mechanism of mineral-microorganism synergistic energy conversion on semiconducting properties and photoelectric conversion efficiency will be also explored to compare the differences in energy conversion pathways and efficiency of mineral photoelectrons and valence electrons in sulfate-reducing bacteria and the relative contributions of these two energy sources in driving carbon, nitrogen and sulfur cycle in the hydrosphere. In addition, it's prospective to discuss the molecular mechanism of electroactive microorganisms filling optical holes of semiconducting minerals, promoting microbial metabolism, and mediating the morphological transformation of carbon and nitrogen elements. Moreover, by analyzing the microbial groups and the mechanism of energy metabolism that utilize photoelectrons of semiconducting minerals, the main microbial groups that can utilize photoelectrons will be determined, which will be expected to quantitatively evaluate the influence and contribution of different energy forms on carbon, nitrogen and sulfur cycle in the natural photocatalytic system of the hydrosphere euphotic zone.

5.2. Molecular mechanisms of photoelectrons uptake by non-phototrophic microorganisms and their impact on carbon, nitrogen, and sulfur cycle in the natural photocatalytic system of the hydrosphere euphotic zone

Although several proteins that are crucial for microbial EET have been identified and extensively characterized in the last decade, the effect of sunlight on the efficiency of EET and the mechanism of intracellular electron transport in dissimilatory metal-reducing bacteria, such as Geobacter and Pseudomonas, within anaerobic environments in the presence of semiconducting minerals remain enigmatic. Multi-omics and photoelectrochemical analyses have been undertaken to explore the pathway and efficiency of electron flow between semiconducting minerals and microorganisms. Specifically, the critical proteins within the cell envelope, such as cytochrome c, play a pivotal role in the light-induced electron transfer process between minerals and microorganisms. Further in vivo and in vitro characterizations are needed to investigate the functions, interactions, and roles of these proteins in the electron transfer at the mineral-microbe interface under light irradiation. Detailed information about the structure and sequences of the proteins will also reveal the fundamentals of electron transfer properties and phylogenetic diversity. Another significant gap in our understanding lies in deciphering whether the molecular mechanism of EET exhibited by the model microorganism S. oneidensis MR-1 applies to other types of microorganisms. Another critical knowledge gap involves determining whether the proposed molecular mechanism of EET observed in the model microorganisms S. oneidensis MR-1 applies to other microorganisms that take up photoelectrons from semiconducting minerals in natural environments. To address these issues, new techniques and methods in the fields of molecular microbiology and bioinformatics need to be developed. Finally, it is essential to evaluate the ecological impact and the contributions of the light-triggered synergy between microorganisms and semiconducting minerals to the biogeochemical cycle of elements on Earth's surface need to be evaluated. From a biotechnological standpoint, a mechanistic understanding of these electron transfer processes at the molecular level will help us to develop more effective semiconductor-microorganism hybrid systems for biofuel production and the mitigation of greenhouse gas emissions.

5.3. Molecular mechanisms of novel EET, cell sensing and adaptation to potential gradient of electroactive microorganisms

This part will concentrate on the process of sensing potential signals from receptors, the transmission pathway of signals in Geobacter, the response of Geobacter induced by potential signals, and the adaptation mechanism of Geobacter to receptor potential. Besides, it will also discuss the composition and structure of the EET chain under different receptor potentials, analyze the composition and structure of the Arc system and the conversion process of potential signal to cell signal, as well as the composition and characteristics of genes regulated by ArcA. In the meanwhile, the molecular mechanism of EET and adaptation to the oxygen gradient of methanotrophs need to be further explored. Establishing a co-culture system between hypoxic methanotrophs and sulfate-reducing bacteria as electron acceptors will provide new insights into the mechanisms of EET. The whole genome and transcriptome data of hypoxic methanotrophs and sulfate-reducing bacteria will be compared to identify differentially significant functional genes closely related to electron transfer and energy metabolism. Systematically, it will further investigate the formation conditions, electron transfer properties, interspecific energy cooperation mechanism, and methane emission reduction capabilities of hypoxic methanotrophs and sulfate-reducing bacteria.

5.4. Formation and structural characteristics of microbial LDET networks and the mechanism of driving element cycle

Microbial LDET networks greatly expand the role of microorganisms, exhibiting great potential in driving element cycles in heterogeneous sediments. Thereinto, the microbial LDET networks with cable bacteria as the core play an important role in regulating greenhouse gas emissions, which would be of great potential significance for alleviating the global warming crisis and realizing the major strategic goal of carbon peaking and carbon neutrality in China. However, so far, the formation characteristics, structural composition, and regulatory characteristics of CB-LDETNs remain unknown, which greatly limits the deep exploration of their ecological potential. It is necessary to further explore the basic characteristics and ecological functions of CB-LDETNs, and then evaluate their contribution to ecological effects.

Overall, the hydrosphere euphotic zone is an extremely complex and open system, which is filled with sunlight, water, organic acids, inorganic salts, minerals, microorganisms, etc., in which a variety of natural processes happening incessantly have not been fully recognized by humans. However, energy and nutrients in the hydrosphere habitat are limited, and oligotrophic and low-energy supply is widespread, which is unlike the abundant energy and nutrients in the terrestrial system. Microorganisms can only obtain different forms of external energy or improve the efficiency of energy conversion through electron transfer with extracellular minerals and other types of species, to survive in a low-energy environment. Therefore, there is no doubt that the new pathways and regulatory mechanisms of energy conversion and metabolism of microbes in the hydrosphere need to be further explored. The energy metabolism mechanism of hydrosphere microorganisms will be further investigated photoelectric conversion efficiency of semiconducting minerals, transmembrane electron transfer pathway of microorganisms, interspecific electron transfer and energy synthesis efficiency, molecular mechanism of microbial perception and adaptation to potential gradient, and structure and function of LDET networks for the special hydrosphere habitats with oligotrophic and low-energy supply. In terms of mineral photoelectron energy, cable microbes and EET, the interfacial electron transfer pathway, interspecific electron transfer chain, energy synthesis, and transformation pathway will be discussed in depth, and the new mechanism of carbon, nitrogen, and sulfur cycle driven by EET of microorganisms in the hydrosphere will also be explored. This research is intended to reveal novel ways, regulation mechanisms, and ecological effects of energy conversion and metabolism of microorganisms, discover new strategies to overcome low-energy supply and improve energy utilization efficiency in typical hydrosphere habitats, and establish an innovative model of microbial energy metabolism in oligotrophic and low-energy supply habitats, which will provide brand-new perspectives for the mechanism of driving carbon, nitrogen and sulfur cycle in the natural photocatalytic system of the hydrosphere euphotic zone.

Acknowledgments

This work was supported by Major Programs of National Natural Science Foundation of China. They are Integration Program (92251301), Key Programs (91851208 and 91851202), General Programs (91751105, 91751109 and 91751112).

Declaration of competing interest

The authors declare that they have no conflicts of interest in this work.

Biographies

Anhuai Lu is the professor in School of Earth and Space Sciences, Peking University, and is the director of Materials and Environmental Mineralogy Research Center. He is the past president of the International Mineralogical Association. Besides, he has twice served as the chief scientist in major scientific frontier fields of the National 973 Program, and is currently the chief scientist of the National Key Research Program. He has been engaged in mineralogy research for a long time, established the research system of environmental mineralogy.

Jia Liu is a PhD candidate in School of Earth and Space Sciences, Peking University, majoring in geomaterial and environmental mineralogy. She focuses on geomicrobiology, and more specifically, the mechanism of synergy between semiconducting minerals and microorganisms in the euphotic zone of the hydrosphere. She has won the highest award for students in the field of geology, Li Siguang Outstanding Student Award.