Electron Transfer in the Biogeochemical Sulfur Cycle

Abstract

Microorganisms are key players in the global biogeochemical sulfur cycle. Among them, some have garnered particular attention due to their electrical activity and ability to perform extracellular electron transfer. A growing body of research has highlighted their extensive phylogenetic and metabolic diversity, revealing their crucial roles in ecological processes. In this review, we delve into the electron transfer process between sulfate-reducing bacteria and anaerobic alkane-oxidizing archaea, which facilitates growth within syntrophic communities. Furthermore, we review the phenomenon of long-distance electron transfer and potential extracellular electron transfer in multicellular filamentous sulfur-oxidizing bacteria. These bacteria, with their vast application prospects and ecological significance, play a pivotal role in various ecological processes. Subsequently, we discuss the important role of the pili/cytochrome for electron transfer and presented cutting-edge approaches for exploring and studying electroactive microorganisms. This review provides a comprehensive overview of electroactive microorganisms participating in the biogeochemical sulfur cycle. By examining their electron transfer mechanisms, and the potential ecological and applied implications, we offer novel insights into microbial sulfur metabolism, thereby advancing applications in the development of sustainable bioelectronics materials and bioremediation technologies.

Keywords: biogeochemical sulfur cycle; cytochrome; electroactive microorganisms; electron transfer; long-distance electron transfer; pili.

Figure 1

Conceptual diagram of the sulfur cycle. (A) Global sulfur cycle. The diagram includes some processes discussed in this review. Arrows indicate sulfur fluxes and pathways of biogeochemical or chemical processes. DMS, dimethyl sulfide; MSA, methyl sulfonic acid; C_org, organic matter; ANME, anaerobic methane-oxidizing archaea; SRB, sulfate-reducing bacteria. (B) The biogeochemical cycle of key sulfur compounds. The schematic representation includes the microbially mediated reactions, half-reaction redox potentials [6,7,8], and functional genes involved in the biogeochemical sulfur cycle [5,9,10,11]. The question mark symbol means that the involvement gene is uncertain.

Figure 2

Schematic phylogenetic tree depicting the distribution of different types of sulfate-reducing microorganisms among major phylogenetic lineages. Note the seven phylogenetic lineages of sulfate-reducing bacteria, two in the archaea and five in the bacteria, and not all of the lineages with members capable of sulfate reduction are shown in the tree. The generic name is showed in red font.

Figure 3

Mechanisms of intercellular electron transfer in consortia of ANMEs (blue) and syntrophic SRBs (orange). (A) Direct interspecies electron transfer via conductive nanowires. (B) Cytochrome-based direct electron transfer proposed for adjacent and/or non-adjacent cells. (C) Transfer of molecular electron shuttles. (D) Incomplete reduction of sulfate in ANMEs and zero-valent sulfur transfer to SRBs.

Figure 4

Mechanisms for syntrophic anaerobic photosynthesis of the green sulfur bacteria Prosthecochloris aestaurii and Geobacter sulfurreducens via direct interspecies electron transfer.

Figure 5

Unique metabolic characteristics of cable bacteria, and mechanism of electron transfer through cable bacterium filaments. (A) Model of electrogenic sulfur oxidation by cable bacteria in sediment, and a schematic view of effects of the cable on sedimentary iron and sulfur cycling. Long-distance electron transfer allows anodic cells in the anoxic zone to oxidize sulfide, and electrons transferred through the cable bacteria to cathodic cells extend into the oxic zone, where they reduce oxygen or nitrate. (B) Scanning electron microscopy images of the cable bacterium filaments show parallel ridges [83]. Schematic of the structure of a cross-section, revealing that the periplasm of cable bacteria contains a network of conductive fibers. (C) Model of long-range electron transfer inside the cable bacterium filament and proposed energy metabolism. Putative interactions between partner bacterium/solid anode and cable bacteria through direct contact or conductive pili.