Using a three-dimensional hydroxyapatite/graphene aerogel as a high-performance anode in microbial fuel cells

Highlights

• A three-dimensional hydroxyapatite/graphene aerogel (HA/GA) as anode of microbial fuel cell.

• HA/GA exhibits high conductivity, large surface area and excellent biocompatibility.

• Hierarchical macroporous structure of HA/GA facilitates bacterial adhesion and substrate diffusion.

• HA could stimulate Shewanella putrefaciens to secrete riboflavin thus improving extracellular electron transfer efficiency.

• Th HA/GA anode can boost the power density of bioelectrochemical systems.

Abstract

Bioaffinity of anode materials is a key factor for the power output of microbial fuel cells (MFCs). Anode surfaces with excellent biocompatibility can facilitate bacterial adhesion, biofilm propagation, and extracellular electron transfer. In this study, three-dimensional (3D) hydroxyapatite/graphene aerogel (HA/GA) was synthesized using a facile three-step method: hydrothermal treatment, dialysis, and freeze-drying. The HA/GA anode presented the excellent biocompatibility of HA and high conductivity of graphene. Moreover, the unique edge-to-edge cross-linked architecture of the HA/GA offered a large surface area for bacterial adhesion. Shewanella putrefaciens can generate more flavins through the introduction of highly biocompatible HA nanocrystals on the graphene sheets, leading to a rapid extracellular electron transfer between the biofilm and anode. An MFC containing a HA/GA anode delivered a maximum power density of 2.38 W m^− 2, which was 1.83 times the power density achieved using a GA anode. Furthermore, MFCs equipped with HA/GA anodes were successfully utilized to drive a series of electrical appliances. The HA/GA anode possessed excellent biocompatibility, large surface area, superior hydrophilicity, and high conductivity, which were conducive for enhancing the surface bioaffinity and accelerating the interfacial charge transfer, thereby improving the electricity generation performance of the MFCs. This study has proven that HA is beneficial for enhancing the interface bioaffinity and that it can be applicable to MFC for high-performance bioelectricity harvesting.

Introduction

Microbial fuel cell (MFC) is a type of bioelectrochemical system that utilizes pure bacterial strains or mixed microbial cultures as biocatalysts to realize direct conversion of organic matter into electrical energy [1]. At present, the MFC technology has attracted great interest owing to its dual functions of electricity generation and pollutant treatment [2], [3]. However, its poor efficiency hinders the practical application of MFCs [4], [5]. Bacterial proliferation and extracellular electron transfer (EET) occur on the surfaces of anodes; therefore, the characteristics of anode materials have a crucial impact on the performance of MFCs [6].

The anode surface is in direct contact with bacterial cells and their EET. The electron transfer path in the anode chambers of MFCs includes two main stages: (i) an electrochemically active biofilm (EAB) transfers electrons to the anode surface through the outer membranes, electron shuttle, or conductive pili [7] and (ii) extracellular electrons flow inside the anode material [8]. In general, anode materials exhibiting excellent biocompatibility can increase the affinity between EABs and anodes, which is beneficial for mitigating the interfacial electron transfer resistance [9], [10]. In addition, anode materials possess superior electronic conductivity, which greatly reduces the internal resistance and facilitates achieving facile electron flow inside anodes [11], [12]. Furthermore, high-performance anode materials should have high bacteria-hosting capability [13]. The larger the number of bacterial cells colonized on anode surfaces, the greater the number of extracellular electrons generated per unit time, which is favorable for enhancing the power output of MFCs [14].

In recent years, three-dimensional (3D) porous anode materials have been widely utilized in MFCs owing to their high specific surface area and excellent electrocatalytic activity [15]. The porous structure of 3D materials can greatly increase the attachment sites for bacterial cells, which helps improve the MFC performance [16]. A series of commercially available 3D metal-based and carbon-based materials, such as nickel foam [17], stainless steel wool [18], carbon felt [19], and carbon fiber brush [20], have been employed and achieved high bioelectricity generation in MFCs. To further improve the biocompatibility and electrocatalytic activity of these 3D materials, carbon nanomaterials [21], conductive polymers [22], [23], metal oxides [24], and organic/inorganic molecules [25] have been widely employed as anode modifiers. In addition, biochar derived from biomass waste, such as pinecone [26], cotton textile [27], chestnut shell [28], and steamed cake [29], has received considerable attention owing to its low cost and high performance. At present, some free-standing 3D carbon nanomaterials, such as graphene aerogel (GA) [30] and carbon nanotube (CNT) sponge [31], have high potential as anode materials. Among these 3D materials, GA exhibits excellent electrical conductivity and large specific surface area; thus, it is considered a promising anode material.

To further enhance the bioelectricity generation of GA, a number of studies have been conducted to improve its conductivity, hydrophilicity, and biocompatibility. Zhao et al. prepared GA doped with Pt nanoparticles to accelerate the EET between bacteria and anodes [32]. The enhanced bioelectricity generation performance of MFC can be ascribed to the superconductivity of Pt nanoparticles. Li et al. developed hydrophilic GA that can promote bacterial adhesion and shorten the MFC startup time [33]. Recent reports have concluded that the improved biocompatibility of anode materials can further enhance the charge transfer efficiency between EABs and anodes. Wang et al. fabricated FeS₂ nanoparticles decorated with graphene to boost the performance of MFCs. Geobacter species can utilize FeS₂ as a long-distance electron transfer pathway, resulting in a more efficient electron transfer [34]. In addition, several studies reported that N-doped carbon materials are beneficial for the riboflavin-mediated electron transfer of Shewanella oneidensis [35]. Simply put, the key issue is to enhance the biocompatibility of GA, which is favorable for building “high-speed railway” of EET at the biotic/abiotic interface. Therefore, to further boost the GA performance, it is critical to integrate biocompatible substances with GA.

As a versatile functional material, hydroxyapatite (HA) has been widely used in biomedical applications [36], [37] and environmental remediation [38], [39]. Compared with other biomaterials, HA exhibits excellent biocompatibility, superb cell adsorption, and interfacial bioactivity [40]. Therefore, HA is expected to enhance bacterial colonization and strengthen the affinity between bacteria and anode surfaces [41]. Herein, a type of HA-incorporated GA (HA/GA) with large surface area and excellent biocompatibility was used in an MFC reactor to construct an efficient biotic/abiotic interface. The HA/GA provided abundant attachment sites for bacterial cells owing to its highly porous structure, and compared with flat anodes, it offered substantially higher bacterial loading capacity. Moreover, HA/GA is more hydrophilic than GA, which facilitates bacterial adhesion. Overall, the enhanced biocompatibility of graphene due to the HA nanoparticles significantly improved the bacterial adhesion and vitality on the anode surface. The EAB secreted more flavins, which can serve as electron shuttles by rapidly transferring electrons from the Shewanella putrefaciens to the anode. Therefore, the MFCs equipped with HA/GA anodes exhibited maximum power density, which was much higher than that of GA-MFCs.