Understanding the complexity of wastewater: The combined impacts of carbohydrates and sulphate on the performance of bioelectrochemical systems

Highlights

• The combination of carbohydrate and sulphate reduced current production.

• Acclimation to carbohydrate and sulphate reduced Geobacteraceae numbers.

• Hydrolysis had a negative impact on coulombic efficiency.

• After acclimation sulphate reduction had a negligible impact on performance.

Abstract

Bioelectrochemical systems (BES) have long been viewed as a promising wastewater treatment technology. However, in reality, the performance of bioelectrochemical systems fed with real (and therefore complex) wastewaters is often disappointing. We have sought to investigate the combined impacts of complex substrates and presence of electron acceptors. In particular, this study illustrates and systematically evaluates the disparity in performance between a BES acclimatised with acetate and those acclimatised with more complex carbohydrates (glucose, sucrose or starch) and in the presence and absence of sulphate. Relative to acetate only, operating with complex carbohydrates reduced current by 73%–87% and coulombic efficiency by 4%–50%. Acclimation with complex carbohydrates seriously impeded the colonisation anode by Geobacteraceae, resulting in substantially reduced capacity to produce current (60.2% on average). Combined acclimation with sulphate further reduced current by 35% on average, and resulted in a total reduction of 83%–93% relative to the acetate control. However, the presence of an electrogenic sulphide-sulphur shuttle meant sulphate had little effect on the coulombic efficiency of the BES. The results indicate that a reduction in current and coulombic efficiency is, at present, an unavoidable consequence of operating a BES fed with complex wastewater. Researchers, designers and policy makers should incorporate such losses in both their plans and their prognostications.

Introduction

Bioelectrochemical systems (BES) are viewed as a promising wastewater treatment technology. In principle, they can remove waste whilst producing energy or valuable chemicals (He et al., 2017; Logan and Rabaey, 2012). Their ability to remove chemical oxygen demand (COD), sulphate, ammonia, phosphate and heavy metal in wastewater has been demonstrated (Coma et al., 2013; Kelly and He, 2014; Liang et al., 2018; Wang and Ren, 2014). However, the potential to be energy positive is what makes BES technology exciting. To achieve this, efficient electron scavenging from wastewater is required. Improvements in reactor configuration (Logan et al., 2015), electrode material (Sonawane et al., 2017) and operation (Kaur et al., 2014) have increased BES performance. However, when fed with real wastewater this performance remains problematic with serious implications for the prospects for BES as a treatment technology.

BESs fed with acetate, a simple readily degradable substrate, can produce high current densities and coulombic efficiencies of up to 0.99 mA/cm² and 100% respectively (Fan et al., 2007; Nevin et al., 2008). Yet, the disparity between the performances of BESs operated on acetate and wastewater is huge. In studies which directly compare acetate to wastewater in the same reactors current density has been observed to decrease by 67% at lab scale (Dhar and Lee, 2014), while power density decreased by 95% at pilot scale of 1000L (Liang et al., 2018). The utilization of wastewater by BES is not just slow, but also incomplete; the coulombic efficiency with raw wastewater is often less than 20% (Pandey et al., 2016).

The use of real wastewaters has implications for the abiotic aspects of these systems, such as low conductivity (typically 1 mS/cm) and pH gradients (Rozendal et al., 2008), as well as the biotic aspects. The biotic factors include: microbial diversity (Stratford et al., 2014); competition (Parameswaran et al., 2009); and substrate heterogeneity (Pandey et al., 2016). The limited performance of wastewater fed BESs is well known (He et al., 2017), but not well understood. There is clearly a need for a more systematic approach to this problem that will take us at least some of the way towards an understanding of the disparity between performance of acetate and wastewater fed BESs (Zhao et al., 2020).

One rational approach to understanding the impact of wastewater complexity on BES would be to start with basic components in wastewater, integrating the most fundamental aspects first, and then stepwise adding more complexity to assemble a full picture of the complex network of interactions in wastewater. Two obvious and important differences between wastewater and acetate medium are: (i) most electron donors in wastewater need to be anaerobically converted into smaller molecules before they can be used by electrogenic microorganisms at the bio-anode (Logan et al., 2019), while acetate is a simple molecules that can be directly used by electrogenic microorganisms; (ii) wastewater usually contains electron acceptors such as nitrite and sulphate that compete and interfere with the electron accepting function of the anode (Ma et al., 2015; Zhang et al., 2013) whereas an artificial acetate media does not. Understanding the interplay between substrate complexity and alternative electron acceptors on the performance of BES is expected to shed some light on the fundamental aspects of the impact of wastewater complexity on this technology.

Anaerobic carbohydrate degradation is a common organic removal process in wastewater treatment. It helps BES to take up complex organics, as electrogenic microorganisms have limited ability of to use complex organics as substrate (Catal et al., 2011; Logan et al., 2019). In BES the rate of carbohydrate degradation through hydrolysis and fermentation is thought to be limiting, reducing the rate at which current is produced (Velasquez-Orta et al., 2011; Zhao et al., 2020). Carbohydrate degradation gives rise to the formation of carbohydrate degrading biomass and can also give rise to methanogenesis; both pathways cause a loss of coulombic efficiency (Lee et al., 2008).

Sulphate is a common electron acceptor in environmental waste streams, and frequently the major alternative electron acceptor in BESs fed with municipal wastewater (Zhang et al., 2013; Petropoulos et al., 2019). However, the products of sulphate reduction such as sulphide and sulphur are potentially electrogenic. Therefore, unlike other terminal electron acceptors such as nitrite or carbon dioxide that often bind electrons permanently, sulphate receives electrons and then delivers them to the anode via direct electrogenic oxidation of sulphur species (Dutta et al., 2009; Sun et al., 2009; Zhang et al., 2014). This pathway can interact with the function of BES, recycling the electrons from sulphate reduction, boosting coulombic efficiency.

Individually the presence of either complex carbohydrate or sulphate as components in the substrate can affect the performance of a BES. However, these two components also interact. With the ability to use a wide range of substrates, sulphur reducers might help BES to utilize complex carbohydrates via alternative processes by forming electrogenic sulphur species (Muyzer and Stams, 2008). This might either: attenuate the accumulation of rate limiting intermediates and products of carbohydrate degradation and recover them as current; or force them into a less efficient electrogenic pathway increasing the disparity of the performance between BES with and without sulphate. Thus, the coexistence of just two fundamental components of wastewater: carbohydrate and sulphate, causes already substantial uncertainty into the performance of BES. Furthermore, and in spite of the simplistic belief that acetate is the most readily degradable organic carbon, acetate degradation itself is not necessarily easy and straightforward. While many sulphate reducers oxidize complex organics to CO₂, there is also a substantial group of incomplete oxidizers that stop at acetate rather than CO₂ (Rabus et al., 2013). Another case in point is the oxidation of acetate by an intricate association between Geobacter sulfurreducens and a hydrogen-utilizing exoelectrogen (Kimura and Okabe, 2013; Dolfing, 2014). It is tempting to speculate that hydrogen utilizing exoelectrogens can take up a similar integrative role by simultaneously removing hydrogen that leaks away during degradation of more complex carbon sources, which in turn may affect acetate degradation by G. sulfurreducens-like electrogens.

The aim of this study is to illustrate and evaluate the combined impact of two representative wastewater components, carbohydrate and sulphate, on the performance of BES, with acetate-acclimatised reactor as positive control. The carbohydrates, in order of increasing complexity, were glucose, sucrose and starch. Glucose is fermentable to produce simple electrogenic compounds and the basic unit for building complex carbohydrates. Sucrose is a disaccharide that consists of two glucose moieties with a glycosidic bond. Starch is a complex carbohydrate that is composed of a chain of glucose molecules with glycosidic bonds. The substrates were provided at concentrations equivalent to 640mgCOD/L, which simulated the COD of high strength domestic wastewater. Wastewater treatment is complex and multifaceted. This study tackles one aspect of this complexity, demonstrating a rigorous and systematic methodology as to how such challenges can be approached.