Green hydrogen from microalgal liquefaction byproducts with ammonia recovery and effluent recycle for developing circular processes

https://doi.org/10.1016/j.jclepro.2021.126834Get rights and content

Highlights

  • Microbial electrolysis produced hydrogen using two microalgal waste effluents.

  • Up to 34.4% of ammoniacal nitrogen was separated to the reactor cathode.

  • Reactor effluent was used to regrow microalgae strains and remove remaining organics.

Abstract

Hydrothermal liquefaction is a promising technology for microalgae-based biofuel production. However, hydrothermal liquefaction’s aqueous wastes have little established reuse, and contain significant fractions of toxic ammoniacal nitrogen. Careful reuse of this waste can assure microalgae-based biofuels are produced with less environmental impact and larger energy efficiency. Microbial electrolysis cells were investigated to valorize this waste product by converting the leftover organics into hydrogen and remove ammonia. Waste hydrothermal liquefaction aqueous phase from two microalgal strains, Tetraselmis sp. and Chlorella sp. were used as feedstocks for hydrogen production in microbial electrolysis cells. Chlorella and Tetraselmis aqueous phase-fed microbial electrolysis cells reach an average current density of 5.1 ± 0.19 A/m2 and 3.8 ± 0.08 A/m2. Compound removal rates and mass removal percentages were also investigated for each feedstock. Acetic acid, propionic acid, ethanol, and glycerol were effectively removed from the aqueous byproduct. Further, microbial electrolysis cells separated up to 34.3% of ammoniacal nitrogen present in the aqueous phase. Charge transfer analysis indicated that proton transfer, not ammonium transfer, contributed to the majority of the hydrogen production in the cathode. Finally, the microbial electrolysis cell effluent was reused to grow the same microalgal strains, leading to the development of a circular biofuel production system. Microalgae regrowth studies using microbial electrolysis cell effluent showed nearly complete removal of total organic carbon, but significantly less removal of total nitrogen. Tetraselmis sp. growth occurred with the Tetraselmis-derived MEC effluent, however, the control medium without effluent produced the most growth. These findings support the possibility of a circular biofuel framework using MECs, but additional constraints, including the removal of inorganic contaminants, are necessary to realize the circular processes.

Introduction

Climate change has been widely regarded in the global scientific community as one of the most pressing environmental problems facing the world, with much of the concern being driven by the use of greenhouse gas emitting non-renewable fuel sources. To date, renewable, carbon-neutral fuel sources have not yet achieved the scale or the cost required to compete with fossil fuels.

Of the feedstocks studied for producing liquid fuels, microalgae represent a promising option because of fast growth rates, low land requirements, and high lipid yields. However, the cost of feedstock production and nutrient requirements remain significant barriers to the commercial success of this feedstock. A techno-economic analysis reported by Davis et al., in 2011 determined that the best-case scenario using a 10% internal rate of return would result in a cost of 2.25 USD per L to produce microalgal oils directly, and upgrading the microalgal oil to biofuel using hydrotreating (Davis et al., 2011). While a more recent techno-economic analysis concluded that microalgae-based biofuels could be feasible at a selling price as low as 1.48 USD per L (Thilakaratne et al., 2014) using catalytic pyrolysis, today’s costs of conventional fuels are much lower.

While improving biomass growth rates is intuitively one strategy to limit costs, new practices have attempted to either increase fuel yields from microalgal biomass or develop new valuable products. Thermochemical processing via hydrothermal liquefaction (HTL) is a process where an aqueous phase containing biomass substrate is heated and pressurized, typically above 250 °C, catalyzing a chemical breakdown of biomass polymers into simple subunits, and separation of the lipids as an oil phase. Many different feedstocks have been used in HTL, ranging from agricultural waste products from livestock, plant residues, plastics, and food wastes (Gollakota et al., 2018; Hongthong et al., 2020). HTL provides several advantages over other thermochemical treatment processes. It often does not require other chemical or thermal preprocessing and can be used on wet biomass, making it of particular interest for microalgal cultures (Chisti, 2019) which have a low solid content (0.5–1%) without prior separation. Microalgae’s popularity as a feedstock for HTL has also been noticed recently as a prime candidate for further research (Tian et al., 2014).

Despite its appeals, HTL still has hurdles before it will see mainstream adoption. One major deterrent is the aqueous waste generated. The HTL aqueous phase (HAP) is a waste product that has little use. HAP can contain high concentrations of organic carbon (Maddi et al., 2016). To minimize the loss of carbon and production of waste via this fraction, HAP recycling has been proposed to some success using biomass including microalgae, where the wastewater is used again as the aqueous phase. An early study by Li et al. recycled HAP from HTL using Salix Psammophila branch residues, resulting in an increase in bio-oil yield from 30.3% to 46.9% (Li et al., 2013). Biller et al. (2016) recycled HAP from dried distillers grains back into their HTL process, reaching an energy recovery of 95% as well as gaining larger crude yields (Biller et al., 2016). Ramos-Tercero et al. also performed a process water recycle study using C. Vulgaris as the feedstock and found that bio-oil yields were higher after recycle, however, total energy recovery yields were lower, yielding 68% after a 7th recycle (Ramos-Tercero et al., 2015). Chen et al. also demonstrated increased bio-oil yields from HTL after aqueous phase recycling while using Spirulina Pletensis powder as the feedstock (Chen et al., 2019). HAP Recycling clearly contributes to increased oil yields, however it still poses a problem. When HAP is recycled, organics continue to accumulate in the aqueous phase, which must be disposed of eventually. This makes HAP recycling only a partial solution for generating cleaner energy production. More recently, a study by Davidson et al. compared several methods of HAP treatment, including condensed phase ketonization and dual-bed steam reforming (Davidson et al., 2019). Davidson et al. first ran the HAP through a multistep cleanup process before energy recovery to minimize catalyst inactivation caused by untreated HAP, suggesting that contaminant removal before HAP conversion could be valuable.

Processes that remove contaminants from HAP while simultaneously producing energy are attractive. For a complex waste like HAP, another intuitive means of treatment is via bioprocessing. Biller et al. (2016) proposed anaerobic digestion as a means of consuming the organics present in the HAP after recycle (Biller et al., 2016). Anaerobic degradability was also supported by a study conducted by Tommaso et al. that suggested that HAP could have an anaerobic degradability up to 84% when HTL was operated at 320 °C (Tommaso et al., 2015). Other approaches have been outlined in a review by Gu et al. (2019). Many of these processes produce methane, a potent greenhouse gas that can be released as fugitive emissions if not properly managed. Energy carriers will have better appeal if they do not pose a risk to the climate.

One technology that has not been used to degrade HAP derived from microalgae is the Microbial Electrolysis Cell (MEC). MECs work by using a microbially colonized surface that produces electrons while degrading organics. The electrons are shuttled to a cathode, where they are combined with protons to form hydrogen. Some HAPs have already been demonstrated in MECs. Shen et al. (2016) used HAP from HTL-treated cornstalk, removing 60% of the organics in the waster water as measured by chemical oxygen demand (COD) (Shen et al., 2016). Shen et al. (2018) used swine manure derived HAP fed to MECs, and showed a maximum removal of 98% of fed COD (Shen et al., 2018). These studies show that significant organics can be removed by MECs from HAPs while also producing hydrogen as a zero-emission fuel.

For protein-rich feedstocks like microalgae, ammoniacal nitrogen (NH3-N) can be generated by HTL under a wide range of temperatures and residence times. Tommaso et al. found that NH3-N appeared in all HAPs from microalgae at a range of conditions, ranging from 0 to 1.5 h at a fixed temperature and varying the temperature from 260 to 320 °C (Tommaso et al., 2015). Biller et al. shows that NH3-N was produced for all five of the feedstocks tested (Biller et al., 2012). Ammonia in aqueous streams require treatment before disposal. Concentration and separation of ammonia can result in the production of valuable products such as fertilizers and cleaners. Primarily created via the Haber process, today’s ammonia production is not sustainable. The Haber process requires a source of hydrogen, which is typically produced by natural gas steam reforming (DOE, 2020). Renewable means of acquiring NH3-N must be developed. NH3-N can be separated using MECs due to the formation of a conjugate acid, ammonium, at neutral pH. In MECs that use a cation exchange membrane, ammonium can migrate from the anode to the cathode, where hydrogen evolution at the cathode increases the cathode pH. The increase in pH deprotonates the ammonium ion, preventing back diffusion through the membrane. NH3-N removal from bioelectrochemical system (BES) effluent can be valuable for not only producing ammonia but for improving reactor performance, as its presence can inhibit current and power production (Kim et al., 2011). NH3-N removal has already been demonstrated in other BESs (Kelly and He, 2014). He et al. was one of the earliest studies to demonstrate ammonium removal in a microbial fuel cell (MFC), achieving ammonium removal efficiency as high as 69.7 ± 3.6% using only ammonium as the electron source (He et al., 2009). Jadhav and Ghangrekar also investigated ammonium removal in MFCs, and demonstrated ammonium removal without the use of organic carbon as well, although coupled with a carbon source the MFCs produced more power than without (Jadhav and Ghangrekar, 2015). Shen et al. referenced earlier in the introduction also demonstrated NH3-N removal from a complex waste as part of their study using MECs and showed a maximum NH3-N removal efficiency of 76.53 ± 0.52% (Shen et al., 2018). Finally, Joicy et al. attempted to understand the requirements for ammonia removal without the use of a carbon source, suggesting that 0.72 mg of nitrite nitrogen per mg of NH3-N and 1.73 mg of total alkalinity as CaCO3 per mg NH3-N were sufficient (Joicy et al., 2019). While these studies uncover some important concepts, they have some gaps in knowledge and desired goals. No NH3-N removal studies in MECs fed with microalgal feedstocks have been demonstrated. Additionally, despite the interest in separating NH3-H from complex feedstocks, the dynamics of NH3-N and charge transfer in MECs that are fed these kinds of complex feedstocks are not well understood.

While BESs remove many organic contaminants from wastes, the effluent from BESs often contains organic byproducts. One study used wastewater from MFC and found that C. vulgaris could grow in MFC effluent at a maximum growth yield of 4.7 g/L (Huang et al., 2017), and doubled biomass yields when NaNO3 was added to improve nitrogen availability in the growth media. NO3 and NH3-N are common nitrogen sources for microalgae regrowth (Perez-Garcia et al., 2011), so either source could be useful. If nitrogen availability is a problem for microalgae growth in BES effluents, HAPs may be a valuable nutrient source. Using microalgae to degrade HAP directly has also been studied previously (Leng et al., 2018). Jena et al. was one of the first studies to characterize HAP and use it to regrow the microalgae Chlorella Minutissima (Jena et al., 2011). When 0.2% of HAP was used, the authors found that regrowth rates decreased by approximately a factor of two. Biller et al. (2012) expanded and supported the findings by Jena et al. by performing microalgae growth studies using four different strains (Biller et al., 2012). They showed that only two strains grew more than the control media when using HAP, requiring at least a 200 fold dilution for improved growth. More recent studies have produced promising results. Kumar et al. performed a similar analysis to Biller et al. but used macroalgae strains instead as the HTL feedstock (Kumar et al., 2019). They found that growth marginally improved in HAP-fed cultivations compared to the control, but used a 200-fold dilution as the most concentrated addition of HAP. Das et al. performed regrowth studies on Tetraselmis sp. using HAP, and found similar results to their control medium when 50% of the nutrients tracked were replaced by those provided by HAP (Das et al., 2020). This required a 300-fold dilution of the HAP. These studies suggest that microalgae growth using HAP instead of control mediums is not ideal without significant dilution, and is not always better. Microalgae growth limitations in HAP may be due to a combination of organic and inorganic composition. Using a MEC on HAP and then using the MEC effluent to grow microalgae, it may be possible to maintain or improve microalgae growth instead of using HAPs directly, simultaneously creating energy as hydrogen in the process. MECs may remove a substantial part of the inhibitors affecting microalgae growth but may leave behind enough nutrients needed for the microalgae growth without supplementation.

To make microalgae a more attractive biofuel feedstock, waste production and net energy consumption needed to create microalgae-based fuels must be reduced in high performing processes. Ammonia production is also nonrenewable and has few renewable alternatives, but represents a significant waste from microalgae fuel production. MECs promise to be a unique platform that can tackle all three goals by creating additional energy as hydrogen, separating ammonia from feedstocks, and by removing troublesome organic contaminants from wastes. However, no study has used high performing MECs on such a waste product from microalgae while tracking the effects of ammonia transfer. Combined with prior regrowth efforts using HAPs, MECs may also be used in part of a circular fuel creation process.

This study investigates HAP conversion in MECs using HAP from two different biofuel feedstocks: Chlorella sp. and Tetraselmis sp. Changes in key chemical species and electrochemical performance were compared for the two HAPs. Charge transfer was also tracked to determine the influence of ammonium ions on the process. The HAP treated in MECs was then used to regrow microalgae, investigating the potential framework for a circular biofuel process.

Section snippets

Formation of HAP products

HAP was generated from microalgal biomass in Pacific Northwest National Laboratory’s (PNNL) bench-scale continuous flow hydrothermal reactor. The reactor system was made of 316L stainless steel and was comprised of high-pressure syringe pumps, tube-in-tube heat exchangers, an inline solids separation vessel, and liquid product collection vessels that also served as liquid-gas separators. Additional details of the reactor system are described in earlier publications (Elliott et al., 2013, 2017).

MEC experimental performance

The two microalgae-derived substrates were characterized by measuring pH, NH3-N concentration, and COD concentration. HAP-C was found to have a pH of 8.82, with 6.6 ± 0.1 g-NH3-N/L, and 79.3 ± 0.17 g-COD/L, while HAP-T was found to have a pH of 8.69, containing 2.6 ± 0.05 g-NH3-N/L, and 43.2 ± 0.17 g-COD/L. These characteristics of the HAPs proved to have some operational advantages over other substrates, notably that the reactors required limited pH adjustment. This can be attributed to the

Conclusions

Green hydrogen is emerging as the first molecule of key significance in the post-covid, renewable economy of the 21st century. The energy sector is undergoing a paradigm shift from fossil fuels to carbon-free fuels. Developing alternative pathways to green hydrogen is paramount to managing carbon emissions in the coming decade, as the world tries to limit the temperature from rising more than 1.5 °C. MEC technologies can play a key role as they can generate green products to meet many of the

CRediT authorship contribution statement

Scott J. Satinover: Formal analysis, Writing – original draft, Writing – review & editing, Scott did most of the MEC experimental work, as well as analysis of the charge transfer, measurement of ammonia and other ions, pH calculations, model development, writing the first draft of the major portion of the manuscript and revisions to the manuscript. Shovon Mandal: Shovon did the algal regrowth experiments. Raynella M. Connatser: Formal analysis, Raynella and Samuel did the GC-MS analysis of the

Declaration of competing interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Acknowledgments

This work was supported by funding from the Laboratory Directed Research and Development Program of Oak Ridge National Laboratory (ORNL), managed by UT-Battelle, LLC, for the U.S. Department of Energy under Contract No. DE AC05-00OR22725. The authors acknowledge funding provided by ORNL to the University of Tennessee, Knoxville via a subcontract, and the support provided by Dr. Costas Tsouris. Scott Jason Satinover was partially supported by the Bredesen Center and the Institute for Secure and

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