Purple phototrophic bacteria as a platform to create the next generation of wastewater treatment plants: Energy and resource recovery

C H A P T E R

12 Purple phototrophic bacteria as a platform to create the next generation of wastewater treatment plants: Energy and resource recovery D. Puyola, V.M. Monsalvob, E. Marina, F. Rogallab, J.A. Meleroa, F. Martı´neza, Tim H€ ulsenc, Damien J. Batstonec a

Department of Chemical and Environmental Technology, Rey Juan Carlos University, Madrid, Spain b Department of Technology and Innovation, FCC AQUALIA, Madrid, Spain c Advanced Water Management Centre (AWMC), The University of Queensland, Brisbane, QLD, Australia

New trends in wastewater treatment The year 2014 was the century year of the activated sludge process. Over this time period, sewage control and treatment have provided multiple benefits to humankind, including disease control, health and life quality improvements in cities, and mitigation of environmental impacts of sludges [1]. However, as with any technological development, wastewater treatment has evolved throughout the century. In the 19th century, major technological developments in wastewater treatment systems included sewers and centralized discharge for disease control [2], carbon and solids removal through activated sludge processes [3], followed in the first half of the 20th century by

Wastewater Treatment Residues as Resources For Biorefinery Products and Biofuels https://doi.org/10.1016/B978-0-12-816204-0.00012-6

filtration - clarification, and in the last half of the 20th century [4]. Each technology iteration requires major investments in infrastructure, and has approximately 50 years of cycle length, corresponding to the maximum lifespan of these infrastructures. New relevant concepts and solutions are currently being developed [5–7]. Major drivers are the reduction in consumption of resources (energy, chemicals) by existing wastewater treatment facilities, and enabling the recovery of valuable resources present in wastewater, promoting a circular economy within wastewater treatment processes [8]. Two major concepts are emerging for new wastewater treatment plants (WWTPs). One is focused on direct concentration of wastewater

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12. Purple phototrophic bacteria as a platform to create the next generation of wastewater treatment plants

constituents into a biological matrix, for further extraction in the form of resources and energy. The other aims to reengineer the activated sludge process to transform WWTPs into wastewater biofactories, enabling production of new valuable resources by biological transformation of wastewater constituents. Verstraete et al. proposed the segregation of wastewater streams into major and minor concentrated and diluted streams [7]. This separation was proposed to be merely physical, through filtration-based treatment. The concentrated stream goes directly to anaerobic digestion for further recovery of energy—as biogas—and nutrients from the digestate. A variant of this concept is the recent Partition-Release-Recovery concept (Fig. 12.1), where the agents for stream separation are microorganisms, which selectively transport C and nutrients from the liquid phase and concentrate them into an organic matrix [9]. The process entails a single-stage biological treatment of the wastewater and has four main discharges: (i) reusable water from the partition stage; (ii) biogas; (iii) stabilized biomass from the release stage; and (iv) solid and/or liquid fertilizers, i.e., nitrogen, phosphorus, potassium (N, P, K), from the recovery stage. A number of microbial agents are feasible to be used in this concept, but particularly those with high nutrient and C assimilation potential and relatively high biomass growth rate are preferable. Heterotrophic bacteria processes with low sludge retention times (A-stage) enable the rethinking of the activated sludge process, where the electrons and energy come from wastewater [10, 11].

Another possibility is the use of light as the energy source for the process, using all the energy for C and nutrient partition. This is the case for photosynthetic bacteria and algae, where almost all the C comes from inorganic sources [12] and purple phototrophic bacteria (PPB), where organic C drives the process [13, 14]. Phototrophic technologies are still under development, and present the following fundamental limitations: energy requirements and C efficiency in heterotrophic bacteria, light energy and footprint limitations in algae, and soluble carbon limitation in phototrophic anaerobes. The wastewater biofactory is another relevant concept where relatively high value bioproducts are identified [1]. The applicability of the enhanced activated sludge process is not limited to the domestic sector, and other implementation platforms are attractive. The key is the production of commodities that can be used as raw materials for agriculture or even direct human use. These commodities include organic acids, alcohols, carbon dioxide, purified nutrients, and metals. Organic acids and alcohols can be produced by nonmethanogenic fermentation and extraction [15], or by syngas fermentation for further reforming [16]. However, these are not intended for domestic stream treatment, being more appropriate for sludges of high strength industrial wastewater treatment. In addition, promising high-value compounds can be obtained, such as polyhydroxyalkanoates (PHA) [15, 17] and exopolysaccharides, such as alginates [18]; even fibers like cellulose can be recovered [1].

FIG. 12.1

Partition-Release-Recovery concept for wastewater treatment with concomitant recovery of nutrients and energy.

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Metabolism of purple phototrophic bacteria

Purple phototrophic bacteria as a core process in novel wastewater treatment plants PPB are ubiquitous in nature. However, their preferred environment is the thermocline of lakes and other water bodies, at a depth between 0.3 and 20 m [19, 20]. In these places, they can grow anaerobically, using infrared light as an energy source. PPB blooms (“red water”) usually appear in lakes with high concentrations of sulfide, where purple sulfur bacteria (PSB) prevail over their congener, purple nonsulfur bacteria (PNSB) [21]. Though PNSB can grow autotrophically using low concentrations of sulfide, PSB are specialized in autotrophic growth [22]. However, oligotrophic or eutrophic environments, such as waste lagoons, are the preferred niche of PNSB, whose heterotrophic metabolism favors their growth over any other phototrophic microorganism [19]. These metabolic features give PNSB a unique ability to grow, prevail, and dominate high-strength water environments, such as wastewater. Since PPB grow in wastewater easily, they have been found in WWTPs. Thus, PPB have been identified in the microbial community of activated sludge [21, 23, 24]. In most cases, this presence is incidental and has been related to the red water phenomenon [21, 22, 25]. However, it has been demonstrated that PPB enhance the performance of activated sludge due to their ability to grow in anaerobic light conditions and survive under aeration conditions [26, 27]. Indeed, wastewater settled in anaerobic conditions and illuminated with infrared light unequivocally gives rise to PPB enrichment [24, 28]. This unique ability to grow anaerobically under light conditions has been used to demonstrate that PPB can be used for wastewater remediation in single-stage reactors [29–31]. Indeed, the Partition-Release-Recover concept has been developed around the idea of using PPB as the key core microbial community of the partition

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stage, instead of other high-growth microbes, such as heterotrophic aerobes and photosynthetic microalgae [9, 13, 14, 32]. PPB organisms can outcompete any other anaerobe under light conditions, even under low substrate conditions [14]. This is possible by enhancing their growth in advanced reactors like photo-anaerobic membrane reactors (PAnMBR) [13, 33]. Light filtration seems to be another key feature of PPB-based partition applications, where the visible-UV light radiation is selectively removed to avoid the growth of other phototrophs [33]. This is especially relevant, since algae and cyanobacteria can produce toxins to outcompete other microbes and also produce oxygen that can be used by other heterotrophs, displacing PPB from the microbial community [34]. Another interesting feature of PPB is their ability to grow under psychrophilic conditions with the same performance as in mesophilic conditions with very low adaptation times (a few days), which promotes their application for wastewater treatment in countries with temperate climates [32]. Other new low-energy wastewater concepts, like anaerobic treatment [6] and mainline anaerobic ammonia oxidation [35], lack this feature. Undoubtedly, the versatile metabolism of PPB is the main explanation of their uniqueness as a core mechanism for next-generation WWTPs.

Metabolism of purple phototrophic bacteria Considering all the metabolic possibilities in nature, PPB are the most versatile organisms on earth, able to grow under five out of eight possible conditions (Table 12.1). The only major metabolic pathway that is not present in PPB is chemolithoheterotrophy, which is well represented by haloarchaea that oxidize sulfur as a source of electrons and energy, having acetate as a source of carbon in hypersaline environments [46]. The other two metabolic pathways

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258 TABLE 12.1

12. Purple phototrophic bacteria as a platform to create the next generation of wastewater treatment plants

Versatile metabolisms of purple phototrophic bacteria. e2 donor

e2 acceptor

PhotoHeterotrophic organoanoxygenic heterotrophy photosynthesis

Organic

CO2 (fixation), H+ (H2 production)

Photo-lithoheterotrophy

H2

CO2 (fixation)

Metabolism

Photo-lithoautotrophy

Process

Carbon source

Redox conditions References

Infrared light

Volatile fatty acids, Anaerobic alcohols, sugars

[36]

[37]

Autotrophic anoxygenic photosynthesis

S2 /S0/S2O23 CO2 (fixation)

Photo-anaerobic Fe2+ oxidation

Fe2+

[39]

Photo-anaerobic H2 oxidation

H2

[40]

ChemoFermentation organoheterotrophy Denitrification

Organic

Aerobic oxidation

Chemolithoautotrophy

Energy source

Nitrification

NH4+

Halophilic S2 oxidation

S2

Organic

CO2

[38]

Chemical Organic

[41]

NO3

Organic

O2

Volatile fatty acids, Aerobic alcohols, sugars, proteins

[43]

O2

CO2

[44]

not represented here are photoorganoautotrophy and chemoorganoautotrophy, which are indeed very rare in nature [47]. In any case, the major feature of the PPB metabolism is the ability to grow autotrophically by fixing CO2 in the pentose phosphate cycle [Calvin-Benson-Bassham (CBB) cycle] [48]. All the metabolic pathways evolve around the CBB cycle, even heterotrophic pathways, where CO2 fixation is used to maintain redox homeostasis rather than using it as the C source [49]. This CO2 capture may be viewed, indeed, as a kind of organoautotrophy or, as pointed out by many authors, mixotrophy [47]. Phototrophic mechanisms are based on the cyclic electron transport chain (ETC), in a process called anoxygenic photophosphorylation,

Anoxic

[42]

[45]

which can reuse and reenergize electrons from a wide variety of electron donors, both inorganics (photoautotrophy) as well as organics (photoheterotrophy). A unique feature of the ETC of PPB is the presence of bacteriochlorophyll as the central part of the light-scattering system, which is able to use near-infrared light (800–1200 nm) as the energy source for energizing electrons in the reaction center [50]. However, PPB are also able to use some parts of the visible light by locally transforming the high-energy photons into infrared photons by the action of carotenoids, which drive these lower energy photons into the reaction center of the bacteriochlorophyll. This, in turn, enlarges the phototrophic ability of PPB [51]. The energy in phototrophic metabolism is obtained by using

IV. New technologies for wastewater treatment and value-added product development

Metabolism of purple phototrophic bacteria

the energized electrons from organic or inorganic sources to create a proton motive force (pmf) in the periplasm that is subsequently used for ATP synthesis [52]. Under phototrophic conditions, PPB can use CO2 as the terminal electron acceptor in the CBB cycle. In contrast, chemoheterotrophic growth in the dark works in a completely different way, as it does not use the cyclic ETC. In this case, anaerobic oxidation of simple organics occurs [41]; even fermentation of sugars is possible by an unusual anaerobic catabolism of sugars, where the terminal electron acceptors are S and N-organic compounds, like dimethyl sulfoxide (DMSO) and trimethylamine-N-oxide (TMAO) [42]. Alternatively, some PPB species, such as Rhodobacter capsulatus and Rhodoplanes serenus, are able to perform denitrification of NO3 and N2O to NO2 and N2, respectively [48, 53]. Beside major metabolic mechanisms, PPB can perform side processes that help its growth in most environments, including water bodies with discontinuous presence of soluble organic

259

compounds and nutrients. Accumulation processes are, therefore, needed to survive under such circumstances. PPB are able to accumulate an excess of organics in the form of PHA [54], and an excess of critical nutrients like P as polyphosphate [55] and S as sulfur globules after sulfide oxidation, which can also be used as alternative electron donors [56]. In addition, another major side mechanism is the ability of PPB to fixate N2 as NH+4 , using the nitrogenase located at the end of the ETC. This process has a double benefit, since PPB can obtain a source of N for growth, but also can release excess electrons in the form of H2 to maintain redox homeostasis [57]. From the wastewater perspective, the metabolic versatility of PPB is of great importance, since these bacteria can be used for the treatment of multiple types of wastewater, or even for multiple-step processes, just by favoring any of the metabolic pathways to obtain the expected result. Every single metabolic mechanism of PPB can be exploited for a useful purpose in wastewater treatment (Fig. 12.2). The most important

FIG. 12.2

The versatility of purple phototrophic bacteria (PPB) in wastewater treatment. Abbreviations: COD, chemical oxygen demand; N, nitrogen; DWW, domestic wastewater; N&P, nitrogen and phosphorus; So, elemental sulfur.

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12. Purple phototrophic bacteria as a platform to create the next generation of wastewater treatment plants

mechanism of PPB is photoheterotrophy. Basically, PPB are able to grow under anaerobic conditions at the same rate as heterotrophic aerobes but without the need for dissipating electrons as inorganic terminal electron acceptors, thus maximizing the electron recycling and the carbon recovery [49]. This is fascinating and opens possibilities to enhance biological wastewater treatment and transform typical WWTPs into wastewater recovery plants, or wastewater biofactories. Almost all the C is assimilated by PPB biomass and can be reclaimed for organic resource recovery, e.g., bioplastics based on PHA [58] or protein generation [59], or for bioenergetic processes, such as anaerobic digestion for biogas production or thermal liquefaction and reformation for the production of thirdgeneration biofuels [9, 16]. The photoautotrophic mechanism, especially in PSB, can be exploited to recover valuable S in the form of elemental sulfur particles from partial sulfide oxidation. Sulfide can be sourced from other biological processes, such as sulfate reduction in high-sulfate wastewaters from the mining, petrochemical, and chemical synthesis industries [60], as well as effluents coming from anaerobic digestion [61]. Additionally, the metabolic versatility of PPB can be used for treating wastewater of seasonal composition without losing performance. This is the case for food processing wastewaters [62, 63]. And, most importantly, PPB are especially suited to recover nutrients (N, P, K) and other substances as per their high assimilative and accumulative capacity, which is key to enabling resource recovery processes. PPB seem to have a lead role in next-technology iterations, as multiple applications of these bacteria are emerging for treating wide typologies of wastewater, from both domestic as well as industrial origins. However, while PPB are promising mediators, light input remains a major drawback as this adds complexity and a range of other limitations. This particularly requires further approaches, as it is a major problem when up-scaling the technology, especially when sun

irradiation is proposed. However, this chapter focuses on how the metabolism of PPB fits with main applications for wastewater treatment. Therefore, a comprehensive analysis of the irradiation factor is needed, and would be interesting to analyze in specific approaches to check how radiation limitations affect the scale of photobioreactors.

Modeling the metabolism of purple phototrophic bacteria Modeling biological processes is a useful tool for predicting the performance of a biotechnological system, thus enabling optimization, scale-up, and process engineering. The quest for a model describing the metabolism of PPB is not an easy task, due to the complex metabolism and the number of external (physical or chemical) parameters to consider that are relevant for the process. Especially, a modeler should consider that it is necessary to describe not only a biochemical space, but also a complex quantum-physics space, and the interactions between both spaces. The emerging use of PPB for wastewater treatment with resource recovery makes this quest a real need, as was identified by Batstone et al. [64]. There are simple kinetic models applied for a specific part of the PPB metabolism, which are suitable for specific situations and, thus, are not universally applicable. Most of the models published so far address the identification of metabolic mechanisms of PPB from a systems biology perspective (including energy, carbon, and redox flows), and are not suited to wastewater treatment without the necessary simplifications. Finally, the application of PPB for wastewater treatment has promoted the development of a mechanistic model focused on the domestic wastewater treatment (DWWT) process. This section analyzes the suitability and differences between these types of models, and their real applicability to PPB applications

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Modeling the metabolism of purple phototrophic bacteria

261

FIG. 12.3 Complexity-applicability analysis of the current models of purple phototrophic bacteria metabolism. Abbreviations: GSMM, genome-scale metabolic models.

in wastewater treatment. An overview of the comparison between the complexity and the applicability of the models analyzed here is depicted in Fig. 12.3.

Single process models All the single process models found are related to the production of biohydrogen by PPB. This is indicative of a potential applicability of this process. Pure culture production of biohydrogen is well represented here. The simplest models use single process equations to explain the growth of PPB strains, including first-order and logistic approximations [65, 66], or a modification of first order using a modified Gompertz model [67]. These models generally do not perform mass balances, and the application is descriptive for the culture conditions (and the specific strain) being used. Other more sophisticated models, applied to a single process (generally biohydrogen

production), include the effect of other factors on the biomass growth. Zhang et al. [68] used a modification of the Droop model, which includes growth limitation by nitrogen, and uses Monod equations to explain the dynamics of two substrates, the biomass and one product. In the Droop model, the growth rate of the microorganism is not only affected by the concentration of limiting nutrients but is also defined by the intracellular concentration of the limiting nutrient. A change from the consumption of one substrate to another is explained by using switch functions. The authors also use a modification of the Droop model by means of the Contois equation instead of Monod’s. In the Contois equation, the apparent half velocity constant increases with the increasing biomass concentration (KS
X, where KS is the true half velocity constant and X is the biomass concentration). Monroy et al. [69] proposed a Monod-based model to explain the growth of PPB and production of H2. The main novelties of this model were: (a) the addition of

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12. Purple phototrophic bacteria as a platform to create the next generation of wastewater treatment plants

a term explaining the substrate uptake for maintenance, (b) the use of a polynomial equation to describe the relationship between the biomass growth rate and the light intensity, and (c) the use of exponential limiting factors related to the pH, temperature, and light intensity. However, as with simple models, this model is not massbalanced and, as such, is not applicable to wastewater treatment.

Metabolic models The potential applicability of PPB to multiple biotechnological processes led to the proliferation of metabolic models that are closely related to the complex metabolism of these bacteria. The models are based on a complex flux of matter and energy in bacteria, and, in some cases, they also include light harvesting and transformation into chemical energy. These models can be classified into partial and global models, depending on whether they focused on a specific part of the PPB metabolism or the general metabolism. Partial models are generally specific and use quantitative data to understand the specific composition of the metabolic network that is being described, including membrane proteins, enzymes, cofactors, and all metabolites. This information is usually collected from previous genomic and proteomic analyses to set the boundary conditions of the model. An example is the description of the ETC made by [52]. They elaborated on the description of the ETC by using specific information about the structure of the membrane, the energy transfer from the light-harvesting complex (LHC), as well as the expression of genes that are involved in regulatory pathways. The model includes thermodynamics (through the Nernst equation) and simplified quantic calculations to set the energy fluxes from the LHC to the ETC, and to predict the dynamics of redox cofactors in the system. Energy transformation (ATP synthesis) is calculated by estimation of the membrane potential and the concentration gradient between the

protons in the periplasmic and the cytoplasmic spaces. The simulations of the model predict up to 16 states among aerobic and anaerobic mechanisms. One key result from this model is the demonstration of a stronger reduction of ubiquinone when the ETC switches from high-light to low-light conditions. Another interesting example is the stochastic simulation of the chromatophore vesicles in the species Rhodobacterium sphaeroides by Geyer et al. [70]. The basis of the model is the discretization of the molecules into two states: binding and unbinding. The quantification of the states kinetics is performed through stochastic simulations. The coupling between the photon energy and the energy transformation in the LHC is set by the simulation of a discretized photon pool and an exciton pool, with different states estimated randomly as explained earlier, and with defined volumes and number of molecules per pool. The average state of these pools determines the connectivity with other pools in the ETC (quinone pool, cytochrome c2 pool, and protons pool), as well as with the proteins in the system (the LHC, the reaction center, the cytochrome bc1 complex, and the ATPase). In another case, the regulation of the photosynthetic gene expression in Rhodobacter sphaeroides is modeled by the AppA/PpsR regulon, which activates or represses the expression of the photosystem (PS) [71]. The model can predict the downregulation and upregulation expression of the photosystem based on the oxygen concentration and on the blue light intensity, as the AppA/PpsR system can interact with oxygen and blue light photons to repress the expression of the PS genes. Global models offer a holistic solution to the whole metabolism of PPB. For this reason, due to the vast number of chemical and genetic expressions to be included, these models usually assume some simplifications, and full metabolic fluxes are not implemented. Two examples of this approach are found at Golomysova et al. [72, 73]. This group uses flux balance analysis (FBA)

IV. New technologies for wastewater treatment and value-added product development

Modeling the metabolism of purple phototrophic bacteria

as the technique for determining the metabolic flux model for the species R. capsulatus. This is performed in two main steps: (a) using metagenomics to know the genetic content and build the biochemical reactions based on this information and (b) defining the optimized function, usually the biomass composition and the growth media. The solution is given by the maximization of the objective function, in this case biomass production, under a given growth media composition and a list of reactions. This technique assumes a quasi–steady-state condition. The model is proposed as a list of metabolic reactions represented in a matrix of stoichiometric coefficients, where the processes and components are defined as biochemical reactions and metabolites, respectively. In this approach, all biochemical reactions are explained by first-order equations. All the predictions of the model are based on deterministic simulations, where at steady state the metabolites do not vary with time, and, therefore, boundary conditions describe a specific steady state. In a first approach, the model was developed with 314 biochemical reactions and 287 metabolites [72], and was further updated to 450 and 500, respectively [73], being capable of predicting photoautotrophic growth, photoheterotrophic growth on acetate, and photoheterotrophic growth on other substrates (such as malate or lactate). The model is focused on biohydrogen production, where the main metabolic fluxes can be predicted by optimization of two objective functions: optimized carbon utilization and optimized hydrogen evolution. Cornet et al. [74] were pioneers in adapting the radiant light transfer into a PPB metabolic model, using Rhodospirillum rubrum as a model organism. They solve the radiation transfer equation (RTE) by one-dimensional geometry, assuming that a semiisotropic intensity distribution exists. The resulting optical radiative properties were calculated for a wavelength range of 350–950 nm. Coupling the light transfer with local kinetic rates was performed by using the local volumetric rate of radiant energy absorbed (LVREA).

263

The calculation includes a Monod-like equation that serves as a limitation for radiation absorption. The spatial coupling was approached by defining two possible spatial states in the reactor: illuminated zones and dark zones. In dark zones, the phototrophic mechanisms are simply not active, as the LVREA is zero. As a limitation of the approach, the metabolism of R. rubrum is explained by a single stoichiometric equation, and only includes biomass growth (including assimilation of P and N, under photoheterotrophic conditions) and polyhydroxybutyrate (PHB) production. Despite the simplicity of the metabolic assumptions, the model is capable of predicting an oscillatory response of the system in terms of biomass concentration. This is explained by an increment and decrement of dark zones in the reactor, which may activate the pigment content regulation. In practice, this affects the biomass retention time. Therefore, this modeling approach can be used under dynamic conditions as a tool for model-based predictive control of heterotrophic photobioreactors operating in continuous mode, but the applicability is limited to PHB production. The height of the metabolic modeling is the use of the entire genome of a specific strain (or even a mixed culture) as a basis for constructing the metabolism. This approach is called genome-scale metabolic modeling (GSMM) and is one of the current paradigms in systems biology. The main limitation of this approach is the need for having all the information regarding the genes encoding all the metabolic proteins. Considering the complexity of PPB, this is challenging. An interesting approach was performed by Imam et al. [75]. They targeted R. sphaeroides as a model organism, creating a manually curated genome-scale metabolic reconstruction, called iRsp1095. This includes 1095 genes (25% of open reading frames), which correspond to 796 metabolites, 858 transformation reactions, and 300 transport reactions. The model is able to predict dark aerobic respiration, dark anaerobic respiration with DMSO as the electron

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12. Purple phototrophic bacteria as a platform to create the next generation of wastewater treatment plants

acceptor, photoheterotrophic growth with a wide range of organic substrates, and photoautotrophic growth with CO2 as the carbon source and H2 or H2S as the electron donor. The model is also able to predict main electron sinks in the process, including hydrogen production and PHA accumulation. The number of potential substrates were 129 carbon sources, 72 nitrogen sources, 46 phosphorus sources, and 9 sulfur sources.

Wastewater treatment model: The PhotoAnaerobic Model no. 1 (PAnM-1) Metabolic models are suitable for an in-depth description of the metabolism of PPB. However, they are not suitable for wastewater treatment due to the following reasons: (a) PPB-based wastewater systems are based on mixed-culture conditions. The actors involved are not limited to PPB metabolic mechanisms, but rely on the interaction between the chemical, biochemical, and physical frameworks, which ultimately define the boundary conditions. (b) A full description of the genome in wastewater treatment is very hard. The computational and analytical effort needed for such an approach makes it unsuitable to define properly the scale of the genomic interactions. (c) Wastewater components are very specific, and usually do not comprise the components needed for the development of a metabolic model. Therefore, any metabolic model would need an interface to engage with the wastewater components. The necessary assumptions for this approach may make the metabolic model unrealistic, as some numerical problems would arise that hinder the convergence of the results. Therefore it is necessary to elaborate a model suitable for wastewater treatment approaches. This was first identified by Batstone et al. [64]

and was materialized in a work by Puyol et al. [76]. The photo-anaerobic model 1 (PAnM-1) was proposed to explain the performance of a mixed culture of PPB treating domestic wastewater. A summary of the model is depicted in Fig. 12.3. The model includes the following mechanisms: (a) Photoheterotrophic uptake with acetate, involving the assimilation of acetate as a carbon source under light conditions. (b) Photoheterotrophic uptake with other organics, involving the assimilation of other organic acids, alcohols, sugars and proteins, lumped as a sole component. (c) Chemoheterotrophic uptake, involving all the fermentative and anaerobic oxidative mechanisms that result in acetate and hydrogen production under dark conditions. (d) Photoautotrophic uptake of CO2, involving H2 as the electron donor of the process under light conditions. (e) PPB decay, which corresponds to cell death and deactivation. (f) Hydrolysis and particulate fermentation, including the decomposition of particulates into soluble components (acetate and others), as well as inorganic release (CO2, H2, N, and P). All uptake processes also include nutrient uptake (nitrogen as NH4+ and phosphorus as PO43 ) (Fig. 12.4). The model is balanced over chemical oxygen demand (COD), C, N, P, and charges (ions). Growth-related processes (a–d) are explained by Monod kinetics, whereas first-order kinetics are used for the description of biochemical processes not related to growth (e–f). Limiting factors were used as in Monod or inverse Monod equations, including limitation by nutrients, light intensity and free ammonia inhibition, as well as competitive inhibition between acetate and other organics. An interesting feature is that this model can predict

IV. New technologies for wastewater treatment and value-added product development

Applications of purple phototrophic bacteria in wastewater treatment

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analysis of the physical relationship between pure cultures of PPB and light energy that may be useful to further upgrade the PAnM-1 [74, 77–79].

Applications of purple phototrophic bacteria in wastewater treatment Domestic wastewater

FIG. 12.4 Schematic summary of purple phototrophic bacteria (PPB) metabolism under domestic wastewater treatment. Key: N2ase, nitrogenase complex; TCA-c, tri-carboxylic acid cycle; DF, dark fermentation; VFA, volatile fatty acids; e, electrons; Dash, electron cycles; Dot, proton pumps; € *, model components. Reference D. Puyol, E.M. Barry, T. Hulsen, D.J. Batstone, A mechanistic model for anaerobic phototrophs in domestic wastewater applications: photo-anaerobic model (PAnM), Water Res. 116 (2017) 241–253, with permission.

electron fluxes by accounting for the COD balance. This makes it easy to implement a metabolic network in this framework. The model is only valid for DWWT in anaerobic conditions. Hydrogen production is considered as inhibited due to high ammonium concentration. There are some limitations of the model that require further upgrading: - The model does not consider accumulation of polyphosphate and its relationship with light intensity. - There is a lack of the description of the accumulation of organics in the form of PHA and glycogen. - Light transfer analysis is lacking. The biomass state is limited to active/inactive. For process optimization, light transfer is particularly important. Finally, there is some

PPB have been applied in DWWT at labscale, though only recent studies have proposed PPB as an alternative to the traditional activated sludge process. H€ ulsen et al. [13] pioneered treating domestic wastewater completely by nonoxidative biological processes by proposing that PPB could be used in a continuous reactor for DWWT. Table 12.2 provides data from some recent applications of PPB for DWWT. PPB mixed cultures clearly dominate the microbial typologies of DWWT, since it is not possible to work under sterile conditions and thus pure culturing does not make sense. The authors of this chapter have an ongoing effort dealing with the scale-up of the technology to achieve a high technology readiness level of 7 (TRL7) using anaerobic open ponds (unpublished, developed by FCC AQUALIA and the URJC, personal communication). However, this is in an early stage of development and the main results will be advanced over the following months. Taking into account the operational variables used in different studies, PPB applications can be developed over a wide range of temperatures (10–30oC), hydraulic retention time (HRT) (8–48 h), and solids retention time (SRT) (2–20 d). The potential application of PPB in DWWT from tropical to temperate regions is possible. Low-temperature operation seems to actually enhance the applicability and capacity of the process, with a low-temperature adapted community having a higher proportion of PPB biomass, and higher activities at moderate temperatures [32]. HRT and SRT are maintained at

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Wastewater characteristics

TCOD (mg/L)

SCOD (mg/L)

Reactor regime

Extra PO4-P COD N (mgN/L) (mgP/L) (mg/L)

Type of reactor

Illumination

HRT Type of T (°C) (h) SRT (d) illumination

Biomass

Light Wavelength intensity Biomass type (nm) (w/m2)

Removal efficiency

Biomass Ef. yield TCOD Ef. N Ef. PO4- Study P (%) reference (% COD) (%) (%)

430–460 241–245 47

6.9

460–711 MBR

22

8–23

2–3.1

Artificial (IR-LED)

Near IR (800–1500)

50

PPB mixed 1.01 culture

96–97

84–92 95–98

[13]

534

348

41

7.2

296–338 MBR

10

12–22 2.7–5

Artificial (IR-LED)

Near IR (800–1500)

50

PPB mixed – culture

87

77

98

[32]

4100

–

–

–

0

Multiple 23–25 24 CSTR

3.2–20

Artificial (100 W incandescent bulbs)

VIS-IR

133

Mixed culture

–

92

–

–

[28]

750

–

6.5

6.5

0

CSTR/ ceramic biofilms

30

48

–

Sunlight

–

–

PNSB

–

88.5

98.5

76.5

[80]

20–30

1–2

0

CSTR

30

24

14

Artificial (60 W incandescent bulbs)

VIS-IR

133

PPB mixed – culture

96–99

76–89 73–88

250–330 80–150

[30]

Key: TCOD, total chemical oxygen demand; SCOD, soluble chemical oxygen demand; HRT, hydraulic retention time; SRT, solids retention time; Ef., efficiency; MBR, membrane biological reactor; CSTR, completely stirred tank reactor; IR-LED, infrared light emitting diode; VIS-IR, visible-Infrared; PPB, purple phototrophic bacteria; PNSB, purple nonsulfur bacteria.

12. Purple phototrophic bacteria as a platform to create the next generation of wastewater treatment plants

IV. New technologies for wastewater treatment and value-added product development

TABLE 12.2 Summary conditions and results for five studies on domestic wastewater treatment by purple phototrophic bacteria (PPB).

Applications of purple phototrophic bacteria in wastewater treatment

very low levels in order to minimize oxidation of organics, while simultaneously assimilating nutrients into the biomass [11]. Increased SRTs decrease the yield [11], which limits nitrogen and phosphorus assimilation. Yet, higher SRT levels (>2 d) are necessary to achieve sufficient COD removal. Due to this, the SRT can be considered a very influential variable in the application of PPB. The range of HRT used was higher compared to conventional activate sludge and biological nitrogen removal systems, but well in line with other anaerobic technologies [81], and lower in comparison to 2–10 days for algae [82, 83]. The capability of PPB to generate energy from light is related to the presence of chlorophyll (Chl) or bacteriochlorophyll (BChl), which are photosynthetic pigments present in various phototrophic organisms. Different pigments allow the organism to utilize different portions of the light spectrum. PPB contain two different pigments: BChl-a (wavelength range of absorption maxima at 375, 590, 805, and 830–911 nm) and/or BChl-b (wavelength range of absorption maxima at 400, 605, 835–850, and 986–1035 nm). A study conducted by H€ ulsen et al. [14] showed a color change in serum flasks from yellow to red within 100 h treating domestic wastewater. The samples taken at this point had developed peaks of light adsorption at 805 and 865 nm, compatible with BChl-a, as well as a peak at 590 nm that was probably related to the carotenoid content causing the change in color [84]. Due to this, there are some studies that have worked exclusively with artificial near-infrared radiation (IR) ([32], others in which artificial light has been used within the visible and infrared range (VIS-IR) [28], and even sunlight [80]. The light intensities used can vary between 50 and 133 W/m2 for the IR and the VIS-IR, respectively. The use of IR LEDs (>800 nm) is a clear energy advantage, since it saves up to 70% energy per photon compared to the UV-VIS range (200–700 nm) [85]. One limitation of DWWT using PPB is insufficient organic C for assimilating all the nutrients

267

(N, P, and K) and maximizing nutrient recovery. Table 12.2 summarizes results from studies where medium- and low-strength domestic wastewaters are fed to PPB reactors. In order to maximize nutrient removal and recovery requirements, it is necessary to provide extra organic COD to promote assimilative removal pathways [14]. H€ ulsen et al. [13] concluded that about 300 mg COD/L should be added as acetic acid to achieve effective removal of nitrogen and phosphorus (>90%) when treating low organic loads. However, there are some cases where the COD/N/P ratio concurs with the ideal PPB ratio (around 100/10/1.5) and extra COD is not necessary [32]. A possible way to optimize nutrient recovery is to promote K accumulation [86] and P accumulation as poly-P [23]. However, the mechanisms for poly-P and K accumulation by PPB are still unknown and more research is therefore needed. There is a possibility of proper functioning of the process with diluted DWWT, since urine streams can be separately treated in decentralized systems [87]. Urine represents approximately 80% of the nitrogen and 45% of the phosphorus present in DWW [88]. If a urine separation efficiency of 50% is achieved, the COD: N:P ratio changes to 100:5.8:1.22, which trends towards ideal values close to 100:6:1. This leads to a viable off-stream to be efficiently treated by a PPB-based process.

Industrial wastewater Industrial wastewater treatment by PPB has been profusely analyzed (see Table 12.3). The list of industries where these bacteria have been tested is extensive: dairy, food processing, textile, brewery, pharmaceutical, latex rubber sheet, palm oil mill, pulp and paper mill, soybean curd, swine or shrimp farm, among others. During the treatment, it is desirable to conserve TCOD and TN via nondestructive assimilation of SCOD, NH4-N, and PO4-P into biomass. However, bioavailability of nutrients and COD

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268

TABLE 12.3

Summary of conditions and results for typical applications of purple phototrophic bacteria (PPB) to industrial wastewater treatment. Ef. PO4-P Ef. TCOD (%) Ef. N (%) (%)

21–49

2.4–3.6

2.3

12

94

–

–

[33]

200

34

1.5–4

Same as PPB mixed culture HRT

48.8–86.8

55–95

75–95

[62]

92.1–94.6

–

–

[89]

Industry Dairy

1700–4000 –

Food

3350

Textile (azo dye)

1000–2000 –

52

3.7

0.21

–

PPB mixed culture

Citric acid

4800–6000 –

30–100

–

Batch

Batch

Rhodobacter sphaeroides >89

–

–

[90]

Food

38,016

–

8

388

10

–

PPB mixed culture

–

–

[63]

Brewery

10,000

–

51

360

Batch

Batch

Rhodobacter sphaeroides 80.6

>99

48

[91]

Pharmaceutical

9450

–

1600

–

Batch

Batch

Rhodobacter sphaeroides 40

–

–

[31]

Sago-starch

5100

–

–

–

Batch

Batch

Rhodobacter palustris

–

–

[92]

Latex

1990

–

298

100

Batch

Batch

Rhodobacter gelatinosus 42–55

–

–

[93]

Palm oil mill

44,100

33,940

–

–

Batch

Batch

Rhodobacter sphaeroides 50.1

–

–

[94]

Palm oil mill + pulp and paper mill

58,750

42,250

–

–

Batch

Batch

Rhodobacter sphaeroides 52.9

–

–

[94]

Soybean curd

3240

–

140

130

3

–

Rhodobacter palustris

77.5

40

>99

[95]

Latex rubber sheet

5800–8000 –

20–35

–

Batch

Batch

Mixed culture + Rhodobacter blastica

90

–

–

[29]

Swine

18,700

–

810

290

Batch

Batch

Rhodobacter palustris

50

–

58

[96]

Shrimp farm

508

–

67

6.1

4

Same as Mixed culture + Rh. HRT palustris

37.4

38.6

57.1

[97]

Dairy

3613

–

409

96.8

–

–

24

17

36.9

[98]

–

PNSB mixed culture

PSB Mixed culture

18–94

77

References

Key: TCOD, total chemical oxygen demand; SCOD, soluble chemical oxygen demand; TN, total nitrogen; TP, total phosphorus; HRT, hydraulic retention time; SRT, solids retention time; Ef., efficiency; PPB, purple phototrophic bacteria; PNSB, purple nonsulfur bacteria.

12. Purple phototrophic bacteria as a platform to create the next generation of wastewater treatment plants

IV. New technologies for wastewater treatment and value-added product development

SCOD (mg/L)

TN TP (mgN/L) (mgP/L) HRT (d) SRT (d) Culture

TCOD (mg/L)

Applications of purple phototrophic bacteria in wastewater treatment

are important. In this regard, a mixed microbial community could be beneficial, with chemoheterotrophs mobilizing nutrients and COD to be taken up by photoautotrophs [99]. We note that the advantage of PPB for wastewater treatment rests in the potential to remove COD, N, and P simultaneously. This advantage is substantially reduced when only COD removal is considered, as aerobic and anaerobic bacteria are much more efficient (no illumination required), and volumetric removal rates are much higher compared to rates achieved in illuminated bioreactors. The wastewater organic load varied between low and high loads, in the summarized batch tests (Table 12.3). The industry that used the wastewater with most organic load was the palm oil mill + pulp and paper mill industry: its maximum value was 58 g/L [94]. The wastewater with the lowest organic load was from the shrimp farm industry, which had a minimum value of 0.5 g/L [97]. The largest amount of TN in industrial wastewater corresponds to the pharmaceutical industry (1600 mg N/L). The PPB R. sphaeroides Z08 was applied for pharmaceutical wastewater treatment. After 1:4 dilutions, a reduction of 50% in COD, biomass yield of 780 mg/L, and specific growth of 0.015/h were observed [31]. The influent with the highest amount of P came from the brewing industry, with a value of 388 mg/L and with a removal efficiency close to 50% [91]. These wastewaters also have some common characteristics, which include the biohydrogen production, high C/N and C/P relationship, which promotes C accumulation and diverse and biodegradable organic composition, which allows producing interesting high value-added organic by-products. In autotrophic conversions, biohydrogen can be produced by photosynthetic microorganisms, that is, microalgae and photosynthetic bacteria (e.g., PPB) that convert solar energy into hydrogen [100]. A photobioreactor (PBR) was developed by Chen et al. [101] to improve the production of phototrophic

269

H2 by Rhodopseudomonas palustris WP3-5 using acetate as the sole carbon source. The PBR was illuminated by combinative light sources, reaching a maximum H2 yield of 62.3%. Vincenzini et al. [102] also studied the behavior of R. palustris. They investigated the potential of PNSB in the photoproduction of hydrogen and biomass containing PHB, under limiting amounts of nitrogen, obtaining a synthesis of 40 mg/L d of PHB and a production of 200 mL/L d of H2 when the experiments were supplemented with 60 mg/L d of nitrogen. In relation to the C/N ratio, the cellulose-rich waste, which is produced by the paper and cardboard industries and textile factories, has a ratio from 173/1 to values higher than 1000/1 [103], while the optimal C/N ratio varies from 20/1 to 30/1 [52]. This high C/N ratio implies a high concentration of residual organic carbon or a high amount of hydrolysates. A moderate C/N ratio (7–10) can be used to obtain a low concentration (less than 1 g/L) of residual carbons and a moderate level of PHA content in the cells (45%–50% w/w) [104]. With respect to energy consumption, the illumination intensity for the PPB tests has been reduced compared to previous studies on domestic wastewater (from 50 and 18 to 20 W/m2, assuming the same illuminated surface) [99], being in line with reported low light intensities [105]. This reduces operation costs of a potential full-scale installation, especially when compared with closed photobioreactors for algal growth [82]. However, efficiency losses for larger-scale installations are yet to be determined. Most of these studies are still under very low technological readiness level (1–2), and the studies mostly consist of exploratory batch tests using sterilized wastewater and pure cultures of PPB species like R. palustris, Rhodopseudomonas blastica, R. sphaeroides, or Rhodocyclus gelatinosus (see Table 12.3). However, in the few cases where mixed cultures were used and biomass control was applied, the efficiency of the process

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12. Purple phototrophic bacteria as a platform to create the next generation of wastewater treatment plants

was really promising, with COD, N, and P removal efficiencies higher than 90% [33, 89], 99 % [91], and 99% [95], respectively. In fact, since 1975 [106], the literature did not advance this topic and not a single setup was aimed for scale-up. The vast majority of studies dealt with artificial wastewaters in limited batch tests and attempts to scale up or operate continuous reactors were lacking. This has changed in the last 8 years, where several authors tried sequencing batch reactors (SBR), photo-anaerobic membrane bioreactors (PAnMBRs), biofilm systems (e.g., in flat plate reactors, unpublished work by the authors at UQ/AWMC), and anaerobic

TABLE 12.4

open ponds (unpublished work by the authors at FCC AQUALIA and URJC), as is discussed later in this chapter.

Resource recovery by purple phototrophic bacteria The versatile metabolism of PPB allows recovering from different wastewaters a wide variety of high value-added resources, like single-cell protein, nutrients (N, P, and K), PHA, carotenoids, and biohydrogen, among others (see Table 12.4).

Potential of purple phototrophic bacteria (PPB) for resource recovery from wastewaters.

Resource

Wastewater types

Strategy

Key metabolic processes

Biomass type

References

Growth and N assimilation

Mixed culture, PNSB culture

[29, 63, 99, 107–109]

Single-cell protein Medium to highly organic wastewater with high N content

Optimize growth

Nutrients (N, P, K)

Domestic wastewater, low-strength wastewater

Optimize nutrients Poly-P accumulation, assimilation N assimilation, K accumulation

Mixed culture, PPB culture

[13, 14, 32]

PHA

Highly organic wastewater with nutrient deficiency

Optimize light delivery

Accumulative VFA as PHA

Mixed culture, PNSB culture

[54, 58]

Carotenoids

Highly organic wastewater

Optimize light delivery

Growth

Mixed culture, PPB culture

[62, 108]

Biohydrogen

Highly organic wastewater with no ammonium

Optimize reduced organic assimilation

Electron dissipation in Mixed culture, nitrogenase PNSB culture

[58, 110, 111]

5-Aminolevulinic acid

Sugar-bearing effluents

Optimize light, adding glycine

Shemin pathway

[112, 113]

S

Anaerobic effluents, mining Autotrophic effluents growth

Sulfide oxidation to S0 Mixed culture, and accumulation. PSB culture

[80, 114]

Au

Mining effluents

TBD

Au3+ reduction via NADH

PNSB culture

[115]

Fe

Electronic waste, landfill leachate

Autotrophic growth

Fe2+ oxidation to Fe3+ and precipitation.

Mixed culture, PPB culture

[116]

Ru

Mining

Optimize growth

Ru biosorption

PNSB culture

[117]

Mixed culture, PNSB culture

Key: Poly-P, polyphosphate; VFA, volatile fatty acids; PHA, polyhydroxyalkanoates; NADH, nicotinamide adenine dinucleotide; PPB, purple phototrophic bacteria; PNSB, purple nonsulfur bacteria; PSB, purple sulfur bacteria. TBD, to be described.

IV. New technologies for wastewater treatment and value-added product development

Resource recovery by purple phototrophic bacteria

Biomass products, like single-cell proteins and carotenoids, greatly depend on the biomass growth and nutrient assimilation. The key option for efficient resource recovery from wastewater is the partitioning of soluble organic matter and nutrients into a concentrated separable solid phase [9]. This can be achieved via biological assimilation, where organic matter, N, and P are removed simultaneously, preferably nondestructively, and incorporated into protein-rich biomass. In addition, there is some evidence indicating that light intensity, photoperiod, and light sources affect the production of proteins and carotenoids, as well as their type [118–120]. PPB contain around 60% of biomass as proteins [106]. The results obtained by H€ ulsen et al. [99] showed that the infrared reactor has the potential to produce around 500 kg of protein-rich biomass-COD per ton of influent COD (assuming the presence of adequate amounts of N and P). This achieves a significantly larger recoverable fraction in wastewater treatment compared to conventional anaerobic (methanogenic) technologies. In relation to the recovery of carotenoids, a study conducted by Azad et al. [121] showed that, when using wastewater from the fishing industry, there was an increase in the amount of carotenoids, soluble protein, and biomass yield. For nutrient recovery, accumulative processes, like poly-P, K accumulation, and N assimilation, must be optimized to maximize recovery potential. Assimilative partitioning of wastewater macronutrients and organics in one solids stream (i.e., biomass) that can be digested in a dedicated process to generate biogas, as well as a concentrated nitrogen and phosphorus stream, might be a major advantage for product recovery [14]. The amino acid composition, when grown on different agro-industrial wastewaters, suggested that PPB could substitute for existing animal feed meals, such as poultry, poultry by-products, rendered meat, soybean, and fishmeal, and maybe even food for humans (depending on the wastewater source, e.g., sugar wastewater) [99].

271

PNSB are the main PPB species that often produce hydrogen [122]. Photofermentative hydrogen production by PNSB was first reported more than 60 years ago [123]. Production of hydrogen has been reported for many PNSB: R. sphaeroides [124, 125], R. capsulatus [126], Rhodovulum sulfidophilum W-1S [127], and R. palustris [128]. PNSB can use organic acids (e.g., acetic, butyric [129], propionic [130], malic [131], and lactic [132]), simple sugars, glucose, fructose, and sucrose, industrial, and agricultural effluents for hydrogen production [110]. Laurinavichene et al. [133] concluded that 17.6 L H2 can be produced from 1 L of distillery waste by dark + photo fermentation using PNSB. Energetic products like PHA and biohydrogen may be enhanced by light delivery optimization. However, metabolic engineering is also necessary to favor metabolic pathways in order to obtain the desired product, as is the case for PHA accumulation and 5-aminolevulinic acid production. PHA is a biopolyester that functions both as an intracellular carbon and energy storage molecule, as well as a sink for reducing redox potential [134, 135]. PHAs have attracted attention as an alternative source to petroleumderived plastics, and their properties, such as biodegradability and biocompatibility, have been extensively studied [136]. PHB is probably the most common type of PHA. Many PNSB, like R. sphaeroides, R. palustris, and R. rubrum, can coproduce PHA and H2 under nutrientlimited conditions [137]. Indeed, Padovani et al. [137] concluded that macronutrient depletion (N and/or P) could help create a stressful growth condition and lead to an extra accumulation of the polymer. However, they observed the higher the cumulative hydrogen volume, the lower the amount of PHB. In their work, they achieved a good level of PHB accumulation and hydrogen production of 175 and 1825 mL/L, respectively, from pretreated olive mill wastewater. Sulfur can be readably recovered from sulfurcontaminated wastewater by promoting autotrophic growth on sulfide to produce elemental

IV. New technologies for wastewater treatment and value-added product development

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12. Purple phototrophic bacteria as a platform to create the next generation of wastewater treatment plants

sulfur globules [80, 114]. Metal recovery is also possible by promoting redox and biosorption processes [115–117]. PPB show potential for future wastewater treatment, for the upgrading and recycling of nutrient resources in the nutrients-energywater-environment nexus [107]. Resource recovery will become an economic driver in cyclic wastewater treatment, and new technologies will be required in place of conventional cradle-to-grave solutions [138].

Perspectives and conclusions The next generation of WWTPs must fulfill six major operative prerequisites to cover current economic, environmental, and social challenges: (1) Nondestructive technologies enabling resource recovery (2) Potential raw matter producer (biofactory) within the concept of circular economy (3) Low greenhouse gas (GHG) emission, or even net GHG consumers (4) Low footprint (5) Diminished sewage sludge production (6) Net energy producer The Partition-Release-Recover concept proposed by Batstone and H€ ulsen [9] seems to be the most promising approach to enable full resource recovery from wastewater, aligning with the circular economy concept. The use of PPB for domestic and industrial wastewater treatment allows fulfilling (theoretically) all these prerequisites successfully. However, there are some challenges that should be solved in order to achieve a better penetration of the PPB-based technology into the waste and wastewater management market. The first approaches to industrializing the PPB technology appeared in Japan during the 1970s [106, 139]. The disappearance of the technology’s industrialization over almost 30 years taught the lesson that something was wrong

with the scale-up, and thus the industry did not see the inherent attractiveness of the PPB metabolism. Several factors hindered the industrial development of PPB technology, as listed here: - The wastewater market was not prepared for a resource-recovery oriented process. Early legislation (if any) focused on wastewater decontamination. Discharge limits were the only parameters that water companies were looking at. - During decades, wastewater treatment and biotechnology were not a working couple, and biological wastewater treatment did not possess a strong scientific basis. This was a critical factor, as the PPB metabolism is quite complex, so biotechnology-based process control is an unquestionable element for PPB-based technology industrialization. - Reactor engineering had to be adapted to this new type of biomass with special features. The key is to maximize the radiative surface to enlarge PPB phototrophic capabilities. Traditional CSTR reactors are not suitable as the depth is quite high for light penetration [106]. However, PPB need a perfect mix for optimizing radiation usage and limiting development of chemotrophic bacteria. Possible solutions to both limitations are the use of anaerobic membrane-based photobioreactors [13, 140] and anaerobic open ponds [141, 142]. - PPB-based applications are assimilative (and not oxidative); thus, all biotechnological solutions should fit with PPB growth and related metabolism. In essence, this means that a wastewater application would be feasible if the PPB are able to assimilate all the organics and nutrients in a single stage. The PPB metabolism can be tuned for a better control of cumulative mechanisms (e.g., PHA and poly-P accumulation) and electron dissipation mechanisms (as N2 fixation or CO2 capture); thereby the C/N/P ratios can be theoretically

IV. New technologies for wastewater treatment and value-added product development

Perspectives and conclusions

modulated. Again, this implies a deep knowledge of PPB metabolic mechanisms. Current metabolic control of mixed cultures is lacking. A jump from pure culturing (which is well studied, as shown in section “Applications of purple phototrophic bacteria in wastewater treatment”) to mixed culturing is still needed. In any case, new trends in wastewater treatment are pushing novel technologies or rethinking old concepts to deal with resource recovery, which is the current paradigm. New research groups are emerging worldwide, and some applications have reached pilot-scale operation. These applications are moving from technological readiness levels of 5–7. In other words, they are placing a launching platform for short- to mid-range industrialization. The main research groups that are currently developing the scaleup of the PPB technology for wastewater treatment are: - The group of chemical and environmental engineering (GIQA) at the University Rey Juan Carlos in Madrid (Spain) and the company FCC AQUALIA, which have developed an open pond technology to treat domestic wastewater. The development of this technology can be seen in a prepilot-scale 1 m3 reactor (Fig. 12.5A) illuminated by artificial IR light (TRL 6), followed by a pilot-scale 35 m3 reactor (Fig. 12.5D, TRL 7), which is sunirradiated. An enlarged version of this technology (up to 500 m3) is currently projected, which will allow a final TRL of 8, very close to commercialization scale. - The Advanced Water Management Centre of the University of Queensland (Australia), which is a pioneer in the remaking of PPB technology. They mainly work at development of MBR reactors for single-cell protein production from food industry wastewater and DWWT. The group is currently working on treating piggery wastewater through a 6  80 L flat plate system (Fig. 12.5B) and on

273

domestic wastewater through a 1 m3 anaerobic MBR system (Fig. 12.5C), all of them through submerged illumination. The goal is a TRL between 6 and 7. - The University Nova de Lisboa in collaboration with the company FCC AQUALIA, under the framework of the European Project INCOVER [142]. They use anaerobic open ponds for treating domestic wastewater and molasses to produce PHA. Two 19 m3 pilot-scale reactors have been operated for more than 1 year, with promising results (which will be published soon). A picture of the pilot-scale reactors can be accessed at the INCOVER webpage (https://incover-project.eu/technologies). The targeted TRL is 7. - The China Agricultural University (Beijing, China). They have developed MBR systems at pilot scale for the treatment of food industry wastewater to produce single-cell proteins and extract other high value-added compounds such as carotenoids, coenzyme Q-10, and bacteriochlorophylls. A prototype is shown in Lu et al. [140]. A TRL of around 5 has been achieved, though it is still under development. Other groups that are developing PPB technology for wastewater treatment at lower scale are the Environmental Technology group of the University of Valladolid (Spain) [143], the Environmental Biotechnology group of the Delft University of Technology (The Netherlands) [144], the Environmental Science Center of the University of Tokyo (Japan) [63, 145], the School of Environment and Natural Resources of The Renmin University of China [146, 147], and the Research Group of Sustainable Energy, Air and Water Technology of University of Antwerpen (Belgium) [148], among others. Most of the scaling-up approaches are indeed supported by the industry. This is precisely the main ingredient for a technology to achieve industrialization. The forecast of technology

IV. New technologies for wastewater treatment and value-added product development

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12. Purple phototrophic bacteria as a platform to create the next generation of wastewater treatment plants

FIG. 12.5 Some prototypes of scaled-up purple phototrophic bacteria (PPB) reactors for wastewater treatment with focus on resource recovery: (A) An artificial-irradiated anaerobic open pond for domestic wastewater treatment constructed by Universidad Rey Juan Carlos (URJC) and FCC AQUALIA (Mostoles, Spain). (B) A flat plate system operated with internal illumination for piggery wastewater treatment, constructed by the Advanced Water Management Centre (AWMC) of the University of Queensland (UQ, Brisbane, Australia). (C) A pilot-scale photo-anaerobic membrane bioreactor (PAnMBR) system with artificial internal illumination for domestic wastewater treatment, constructed by the AWMC of the UQ (Brisbane, Australia). (D) An infrared (IR) light-selected sun-irradiated anaerobic open pond for combined domestic wastewater and liquefied organic waste treatment with focus on polyhydroxyalkanoate (PHA) and fertilizer production, constructed by FCC AQUALIA (Toledo, Spain).

development seems to be clear, particularly in Europe (supported by the European Commission through H2020 and H2030 programs), Australia (through funds from the Cooperative Research Centres Program) and China (mainly supported by the Ministry of Agriculture). It

does not seem too preposterous to forecast a future with plenty of purple reactors spreading around big cities and rural areas, where the urban and agricultural waste will become raw matter for the bioindustry to refeed the cities: a true circular bioeconomy.

IV. New technologies for wastewater treatment and value-added product development

References

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