Long-term photosynthetic CO2 removal from biogas and flue-gas: Exploring the potential of closed photobioreactors for high-value biomass production

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60 61 62 63 64 65 Long-term photosynthetic CO2 removal from biogas and flue-gas: exploring the potential of closed photobioreactors for high-value biomass production Alma Toledo-Cervantes1,2, Tamara Morales1, Álvaro González1, Raúl Muñoz1, Raquel Lebrero1* 1.-Department of Chemical Engineering and Environmental Technology, Valladolid, Dr. Mergelina s/n., Valladolid 47011, Spain. 2.- Department of Chemical Engineering, CUCEI-Universidad de Guadalajara, Blvd. M. García Barragán 1451, C.P. 44430, Guadalajara, Jalisco, México. *Corresponding author: r[email protected]s *Title Page *Graphical Abstract Highlights  CO2 abatement from biogas and flue-gas was studied in a tubular photobioreactor  A feast-famine regime was applied for continuous production of high-energy storage compounds  CO2 removals > 98% and complete C and N recovery as biomass was achieved  Microalgae consumed nitrogen in the dark period regardless of the N source  The N-dark feeding strategy increased the carbohydrates productivity by 1.7 times *Highlights (for review : 3 to 5 bullet points (maximum 85 characters including spaces per bullet point) 1 Long-term photosynthetic CO2 removal from biogas and flue-gas: exploring the 1 potential of closed photobioreactors for high-value biomass production 2 3 Alma Toledo-Cervantes1,2, Tamara Morales1, Álvaro González1, Raúl Muñoz1, Raquel 4 Lebrero1* 5 6 1.-Department of Chemical Engineering and Environmental Technology, Valladolid, 7 Dr. Mergelina s/n., Valladolid 47011, Spain. 8 2.- Department of Chemical Engineering, CUCEI-Universidad de Guadalajara, Blvd. 9 M. García Barragán 1451, C.P. 44430, Guadalajara, Jalisco, México. 10 11 *Corresponding author: r[email protected]s 12 13 14 *Manuscript (double-spaced and continuously LINE and PAGE numbered) Click here to download Manuscript (double-spaced and continuously LINE and PAGE numbered): Manuscript Toledo-Cervantes_2018.docxClick here to view linked References 2 Abstract 15 The long-term performance of a tubular photobioreactor interconnected to a gas 16 absorption column for the abatement of CO2 from biogas and flue-gas was investigated. 17 Additionally, a novel nitrogen feast-famine regime was implemented during the flue-gas 18 feeding stage in order to promote the continuous storage of highly-energetic 19 compounds. Results showed effective CO2 (~98%) and H2S (~99%) removals from 20 synthetic biogas, supported by the high photosynthetic activity of microalgae which 21 resulted in an alkaline pH (~10). In addition, CO2 removals of 99 and 91% were 22 observed during the flue-gas operation depending on the nutrients source: mineral salt 23 medium and digestate, respectively. A biomass productivity of ~8 g m-2 d-1 was 24 obtained during both stages, with a complete nitrogen and carbon recovery from the 25 cultivation broth. Moreover, the strategy of feeding nutrients during the dark period 26 promoted the continuous accumulation of carbohydrates, their concentration increasing 27 from 22% under normal nutrition up to 37% during the feast-famine cycle. This 28 represents a productivity of ~3 g-carbohydrates m-2 d-1, which can be further valorized to 29 contribute to the economic sustainability of the photosynthetic CO2 removal process. 30 31 Keywords: Algal-bacterial technology; Biogas upgrading; Carbohydrates production; 32 CO2 abatement; Photobioreactors. 33 34 3 1. Introduction 35 Carbon dioxide (CO2) represents nowadays the most important greenhouse gas (GHG), 36 with 77% of the total GHG emissions worldwide and an annual atmospheric 37 concentration increase of 0.5% over the last decade (López et al., 2014). In addition, the 38 amount of CO2 emitted from anthropogenic sources has increased from 22 Gt in 1990 to 39 33 Gt in 2010, and it is expected to reach 41 Gt by 2030 (World Bank, 2014; United 40 Nations, 2015). From these anthropogenic CO2 emissions, 93.5% are produced from 41 the combustion of fossil fuels, with a typical concentration in the emitted gases ranging 42 from 5 to 20% (Raeesossadati et al., 2014; Warmuzinski et al., 2014). Energy 43 production from biogas also constitutes an important source of anthropogenic CO2 44 emissions (CO2 content in raw biogas can vary from 15 up to 60%), which production 45 in Europe is expected to reach 18-20 million m3 by 2030 (Muñoz et al., 2015). The 46 detrimental effects of this GHG on the environment (i.e. global warming, modification 47 of the pH of oceans, etc.) demand the implementation of cost-effective technologies for 48 CO2 removal from industrial emissions. In the particular case of biogas, the abatement 49 of the CO2 not only entails environmental benefits but also contributes to the upgrading 50 of this biofuel, decreasing its transportation costs and increasing the energy content. 51 Conventional physical/chemical technologies for CO2 removal from flue-gas or biogas, 52 such as scrubbing, adsorption, or cryogenic separation, have been widely implemented 53 due to the extensive knowledge on their design and operation and the high removal 54 efficiencies achieved. However, only biological technologies offer a low environmental 55 impact, besides reducing the operating costs associated to the treatment process. In this 56 regard, CO2-capturing biotechnologies supported by the photosynthetic activity of 57 microalgae in photobioreactors allow for the removal of CO2 in a cost-effective, 58 environmentally friendly way (Raeesossadati et al., 2014; Muñoz et al. 2015). In this 59 4 microalgae-based process, the CO2 is transferred from the gas to the liquid phase when 60 the flue-gas/biogas is sparged into the cultivation broth, being subsequently fixed by 61 microalgae during photosynthesis in the presence of light. Therefore, the CO2 is not 62 only removed from the gas preventing its emission to the atmosphere, but the C-CO2 is 63 recovered as valuable algal biomass, which can be further valorized (Raeesossadati et 64 al., 2014; Muñoz et al. 2015). Moreover, the necessary nutrients for microalgae growth 65 can be supplemented from wastewaters, which increases the environmental 66 sustainability of the process (Park and Cragss, 2010). However, most wastewaters are 67 characterized by a low C/N/P ratio compared to that needed for microalgae growth 68 (20:8:1 for urban wastewaters vs 106:16:1 to ensure balanced algae growth), therefore 69 carbon limitation usually hinders nutrient recovery from wastewater. In this sense, CO2 70 supply into the cultivation broth from biogas or flue-gas increases the availability of 71 inorganic carbon, enhancing biomass productivity, ensuring complete nutrient recovery 72 from wastewater and mitigating microalgae pH-derived inhibition (Arbid et al., 2013; 73 Posadas et al., 2015). 74 The potential of algal-bacterial symbiosis for biogas (Toledo-Cervantes et al., 2016; 75 Toledo-Cervantes et al., 2017b) or flue-gas (Posadas et al. 2015) purification combined 76 to wastewater treatment has been already studied and demonstrated in open 77 photobioreactors. However, few studies have focused on the implementation of this 78 process in closed photobioreactors, which offers higher photosynthetic efficiencies by 79 avoiding light limitation, enhanced biomass productivities and better CO2 mass transfer 80 (Chisti, 2007; Arbid et al., 2013). On the other hand, this photosynthetic CO2-abatement 81 process can be further optimized by implementing nutrient supplementation strategies to 82 promote the production of storage compounds in the algal biomass (Mooij et al., 2013). 83 In this context, the production of a biomass with a high content in the metabolites of 84 5 interest will increase the economic sustainability of the process (Toledo-Cervantes et 85 al., 2017a). 86 This work aimed at evaluating the long-term performance of a tubular photobioreactor 87 interconnected to a CO2 absorption column for the abatement of CO2 from biogas and 88 flue-gas. Furthermore, a feast-famine regime was implemented in order to exploit the 89 cyclic nitrogen absence for the continuous production of high-energy storage 90 compounds. 91 92 2. Materials and methods 93 2.1 Experimental system 94 The experimental system consisted of a tubular photobioreactor interconnected to a 95 mixing chamber and a CO2 absorption column (AC) (Figure 1). The tubular 96 photobioreactor was composed of 12 tubes of 6 cm inner diameter and 94 cm of length, 97 with a total volume of 45.5 L. The mixing chamber (60 cm height, 50 cm width and 35 98 cm length) had a working volume of 60 L. The absorption column was 2 m height (1.73 99 m water column) with an internal diameter of 5 cm and a working volume of 3.5 L. Two 100 sets of high intensity LED PCBs were placed at both sides of the photobioreactor to 101 provide a photosynthetic active radiation (PAR) of ~1100 μmol m-2 s-1. Light:dark 102 cycles of 12:12 h of the PAR were fixed. The cultivation broth was re-circulated 103 through the tubular photobioreactor and the mixing chamber at a linear velocity of 0.5 104 m s-1. The absorption column was operated by supplying co-currently the cultivation 105 broth from the mixing chamber and biogas/flue-gas (through a stainless steel diffuser of 106 2 µm pore size) at the bottom of the column. The operating parameters such as liquid 107 and gas flow rates of the absorption column and nutrients/digestate solution flow rates 108 are described in section 2.2. 109 6 110 2.2 Experimental system operation 111 2.2.1 Operation with biogas (A): 112 Prior operation, an abiotic CO2/H2S removal test was performed in order to determine 113 the optimum liquid to gas flow rates (L/G) ratio in the AC, which maximizes the CO2 114 and H2S removal from biogas without compromising the CH4 content and the quality of 115 the upgraded biogas due to N2 and O2 desorption (Toledo-Cervantes et al., 2016). The 116 biogas used was a synthetic mixture of 29.5% CO2, 0.5% H2S and 70% CH4. The liquid 117 phase was a modified Bristol medium (final pH = 7.5) (g L-1): NaNO3 (1.5), CaCl2 118 2H2O (0.025), MgSO4·7H2O (0.075), K2HPO4 (0.075), KH2PO4 (0.175), NaCl (0.025), 119 and 1 mL L-1 of a micronutrient solution (2.86 g L-1 H3BO3, 1.81 g L-1 MnCl2 4H2O, 120 0.22 g L-1 ZnSO4 7H2O, 0.39 g L-1 Na2MoO4 2H2O, 0.079 g L-1 CuSO4 5H2O and 49.4 121 mg L-1 Co(NO3)2 6H2O). The liquid recirculation rates tested were 60, 150, 300 and 450 122 mL min−1 while the biogas flow rate was set at 40 mL min-1. Hence, L/G ratios ranging 123 from 1 to 11 were studied. The AC was allowed to stabilize for two times the hydraulic 124 retention time prior monitoring the upgraded biogas composition by GC-TCD. 125 126 The system was inoculated with the microalgae Acutudesmus obliquus at an initial 127 suspended solids concentration (SST) of 0.1 g L-1, and operated for biogas upgrading 128 during 150 days. The CO2 contained in the synthetic biogas previously described was 129 used as carbon source for microalgae growth, while nutrients were supplied by means of 130 the modified Bristol medium. During stage IA (from day 1 to 54) the synthetic biogas 131 was fed during the illuminated period into the absorption column at a flow rate of 40 132 mL min-1 and the liquid broth was recirculated through the AC at a flow rate of 400 mL 133 min-1 (L/G ratio = 10). The modified Bristol medium was fed into the mixing chamber 134 13 conditions, the upgraded biogas had a similar composition of that obtained in stage IA: 283 CO2 1.8 ± 3.4%, H2S 0.00 ± 0.00, O2 9.6 ± 3.3%, N2 6.0 ± 2.2% and CH4 82.6 ± 3.8% 284 (Figure 2b). The slightly higher oxygen concentration recorded in the upgraded biogas 285 was correlated with the higher DO concentration in the cultivation broth (10.8 ± 1.2 mg-286 O2 L-1) when compared to stage IA. 287 Regarding algal biomass production, the photobioreactor operation at a HRT = 50 d 288 during stage IA lead to a biomass productivity of 2.5 ± 0.2 g m-2 d-1, which entailed 289 nitrogen and carbon recoveries of 56.6 ± 3.1% and 50.5 ± 4.5%, respectively. In stage 290 IIA, the lower HRT of 25 days resulted in an increase in biomass concentration from 1.6 291 ± 0.1 to 2.2 ± 0.1 g L-1, that corresponded to a biomass productivity of 7.2 ± 0.3 g m-2 d- 292 1. During this period, the mass balance showed that 86.2 ± 2.6% of the C-CO2 removed 293 from biogas and 81.4 ± 3.2% of the nitrogen fed were recovered as biomass. Finally, in 294 stage IIIA, the doubling of the carbon load during the illuminated period allowed 295 increasing the biomass concentration to 2.5 ± 0.1 g L-1 together with a biomass 296 productivity of 8.0 ± 0.2 g m-2 d-1. Under these conditions, a complete nitrogen and 297 carbon recovery as algal biomass was observed. These results confirm the potential of 298 tubular photobioreactors for effective C-CO2 recovery from biogas and nutrients 299 removal. Furthermore, closed photobioreactors are recognized for the higher biomass 300 productivities achieved in comparison with open systems. However, due to the lack of 301 standardization of the reported values, volumetric productivities (g L-1 d-1) are often 302 used for closed photobioreactors instead of areal productivity (g m-2 d-1), which hampers 303 a fair comparison between both configurations. In this sense, while productivities of 304 0.06 g L-1 d-1 have been reported for closed photobioreactors treating biogas (Meier et 305 al., 2016), productivities in the range of 2.2 – 15 g m-2 d-1 are commonly achieved in 306 open systems, which in fact represents volumetric productivities between 0.015 and 0.1 307 14 g L d-1 (Toledo-Cervantes et al., 2016; Posadas et al., 2017; Toledo-Cervantes et al., 308 2017). In this study, the biomass productivity of 8.0 g m-2 d-1 was equivalent to a 309 volumetric biomass productivity of 0.18 g L d-1, which exceeds previous values 310 reported for open systems. 311 312 3.2. High-value algal biomass production from flue-gas 313 Microalgae are capable of producing high-energy compounds, which can contribute to 314 the economic viability of the photosynthetic CO2 removal processes either from biogas 315 or flue-gas. Carbohydrates accumulation triggered by nitrogen starvation is one of the 316 most effective ways to obtain added-value biomass (Ho et al., 2015). It is important to 317 highlight that this operation is performed batch-wise, since a previous biomass 318 production stage is typically required before inducing such accumulation due to the 319 different nutrient requirements of both biochemical processes. In this sense, the concept 320 of “survival of the fattest” introduced by Mooij et al. (2013) was here applied as a 321 strategy to induce the continuous accumulation of high-energy storage compounds in 322 the produced microalgae while cleaning flue-gas. 323 In stage IB, the biogas fed during operation stages IA-IIIA was replaced by a synthetic 324 flue-gas containing 20% of CO2; therefore, the mineral medium was modified 325 accordingly in order to balance the carbon/nitrogen load to keep the same assimilative 326 nutrient removal reached in section 3.1.2. Consequently, the nutrient solution was fed at 327 an HRT of 15 days and the system was operated until constant biomass concentration of 328 1.5 ± 0.0 g L-1 was achieved. Under steady conditions, ~100% of the N-NO3 fed and the 329 C-CO2 removed from flue-gas were recovered as biomass (Table 2). The harvested 330 biomass, corresponding to the total effluent obtained at the end of the alimentation 331 15 period (i.e. after the light period), reached 8.3 ± 0.2 g m-2 d-1, with a composition of 332 ~22.1% carbohydrates, 48.3 % proteins and 14.6 % ashes (Table 3). 333 During stage IIB, the nitrogen source was removed from the mineral medium while 334 maintaining the same nutrients load (Figure 3). The latter strategy was implemented in 335 order to decrease the nitrogen concentration in the cultivation broth to a non-336 assimilative concentration of ~1.3 mg-N L-1 in which the accumulation of high-energy 337 compounds such as lipids and/or carbohydrates can occur (Figure 3). 338 Once N concentrations <2 mg-N L-1 were achieved in the cultivation broth, the mineral 339 medium was supplemented with N-NO3 and fed only during the dark period at the 340 required nitrogen load to keep the same biomass productivity of that recorded in stage 341 IIB (Table 2). As can be observed from Figure 3, microalgae were initially not able to 342 consume the nitrogen in the absence of light (days 297-320 of stage IIIB). This can be 343 explained by the fact that nitrogen assimilation requires the fixed CO2 and the energy 344 generated in the photosynthetic process. Moreover, to assimilate nitrate, the molecule 345 has to be transported across the membrane and be reduced to ammonia, consuming in 346 the process large amounts of energy, carbon, and protons (Perez-Garcia et al., 2011). 347 After this initial adaptation period of ~20 days, consumption of the supplied nitrogen 348 during the dark phase was observed from day 320 onwards. This fact was attributed to 349 the concomitant degradation of storage starch in the dark period. This phenomenon 350 would require a regenerative cycling of adenine nucleotides and phosphate that can be 351 supported by chlororespiration, which plays an important role in the dark recovery of 352 plants from photoinhibition through de novo protein synthesis (Beardall et al., 2003). It 353 has been suggested that chlororespiration supplies ATP for maintenance and synthetic 354 processes in chloroplasts in the dark, supplementing ATP from glycolysis in the plastids 355 (Raven and Beardall, 2003). Therefore, the accumulated high-energy molecules in the 356 16 form of glucose-based carbohydrates might be oxidized through the Embden–Meyerhof 357 pathway and/or the Pentose Phosphate pathway, the energy production routes (NADPH, 358 ATP), during the dark period. In that way, enzymes involved in nitrate assimilation 359 (nitrate reductase and nitrite reductase) that work sequentially, had the required energy 360 to catalyze nitrate to ammonium in the dark period; while during the light period CO2 is 361 reduced to carbohydrates through the Calvin cycle. This hypothesis was supported by 362 the higher carbohydrate content recorded by the end of the light period, i.e. the 12 h 363 nitrogen famine period, in contrast to that recorded by the end of the dark period, i.e. the 364 12 h nitrogen supplementation period (Table 3). 365 Similar results were observed during stage IVB, when the mineral medium was replaced 366 by an anaerobic digestate but keeping the same nitrogen (N-NH4+) load. At this point, it 367 is worth noticing that the variation in biomass productivity observed in stage IVB was 368 likely due to the decrease in CO2 removal down to 91.6± 11.3%, driven by the lower pH 369 as a result of ammonium feeding. Furthermore, during this period the occurrence of 370 Pseudanabaena sp. (12%) was recorded which was attributed to lack of aseptic 371 conditions of the digestate. This fact is frequently reported in open systems where rapid 372 variations in microalgae population are expected. Moreover, the appearance of this 373 cyanobacterium has been previously reported in wastewater treatment processes 374 coupled to biogas upgrading (Serejo et al., 2015). 375 Finally, carbohydrates productivities ~3 g m-2 d-1 were recorded under the N-dark 376 feeding strategies, which represents 1.7 times the productivity reached under normal 377 nutrition conditions (Figure 4). The high concentration of carbohydrates reached is 378 preferred for its chemical or biological valorization, for instance as the substrate for 379 biohydrogen by dark-fermentation (Chen et al., 2016), ethanol (John et al., 2011) or 380 biogas production (Zamalloa et al., 2011). Furthermore, the biomass production through 381 17 wastewater treatment significantly contributes to the flue-gas or biogas cleaning process 382 (Toledo-Cervantes et al., 2017a.). These results confirm the feasibility of applying this 383 novel strategy for inducing the accumulation of high-energy storage compounds during 384 the photosynthetic abatement of CO2 coupled with wastewater treatment, since it allows 385 for a continuous production of added-value algal biomass. 386 387 4. Conclusions 388 To the best of our knowledge, this is the first experimental study reporting the long-term 389 performance of a tubular photobioreactor for the abatement of CO2 from exhaust gases 390 (biogas and flue-gas) coupled with algal biomass production. The system here proposed 391 showed an efficient removal of CO2 from gas streams (>98%), the upgraded biogas 392 composition meeting the required standards for electricity production. Moreover, the 393 innovative nutrient supplementation strategy, i.e. feeding nutrients during the dark 394 period, allowed enhancing the carbohydrates content in the produced biomass by 1.7 395 times regardless of the nitrogen source. In summary, this study confirmed the potential 396 of the photosynthetic CO2 removal process in closed photobioreactors to support 397 nutrient recovery from digestate and production of added-value biomass with high 398 carbohydrates content, resulting in a cost-efficient and environmentally-friendly 399 technology. 400 401 Acknowledgments 402 This work was supported by the research grants of the Fundación Iberdrola, the 403 Regional Government of Castilla y León (UIC 71), MINECO and the European Union 404 through the FEDER program (CTM2015-70722-R). CONACyT-México is gratefully 405 acknowledged for the Postdoctoral grant of Alma Toledo (No. Reg: 237873). 406 18 407 References 408 1. Arbid Z., Ruiz J., Álvarez-Díaz P., Garrido-Pérez C., Barragán J., Perales J. A., 409 Effect of pH control by means of flue gas addition on three different photo-bioreactors 410 treating urban wastewater in long-term operation. Ecol. Eng. 2013, 57: 226-235. 411 2. Beardall, J., Quigg, A., & Raven, J. A. 2003. Oxygen consumption: 412 photorespiration and chlororespiration. In Photosynthesis in algae. pp. 157-181. 413 Springer Netherlands. 414 3. Chisti, Y., Biodiesel from microalgae. Biotechnol. Adv. 2007, 25: 294–306. 415 4. Chen, C. Y., Chang, H. Y., & Chang, J. S. Producing carbohydrate-rich 416 microalgal biomass grown under mixotrophic conditions as feedstock for biohydrogen 417 production. International journal of hydrogen energy, 2016, 41(7), 4413-4420. 418 5. Perez-Garcia, O., Escalante, F. M., de-Bashan, L. E., Bashan, Y. Heterotrophic 419 cultures of microalgae: metabolism and potential products. Water research, 2011, 45(1), 420 11-36. 421 6. Dubois, M., Gilles, K.A., Hamilton, J.K., Rebers, P.A., Smith, F., Colorimetric 422 method for determination of sugars and related substances. Anal. Chem. 1956, 28:, 350–423 356. 424 7. Eaton, A.D., Clesceri, L.S., Greenberg, A.E. Standard Methods for the 425 Examination of Water and Wastewater, 21st ed. American Public Health 426 Association/American Water Works Association/Water Environment Federation, 427 Washington, DC, 2005. 428 8. Franco-Morgado, M., Alcántara, C., Noyola, A., Muñoz, R., González-Sánchez, 429 A., A study of photosynthetic biogas upgrading based on a high rate algal pond under 430 19 alkaline conditions: Influence of the illumination regime. Sci. Total Environ. 2017, 592: 431 419–425. 432 9. González-Sánchez, A., and Posten C. Fate of H2S during the cultivation of 433 Chlorella sp. deployed for biogas upgrading. J. Environ. Manage. 2017, 191: 252-257. 434 10. Grobbelaar, J.U. 2013. Inorganic Algal Nutrition, in: Richmond, A., and Hu, Q. 435 (Eds), Handbook of Microalgal Culture: Applied Phycology and Biotechnology; 2nd 436 edition, John Wiley & Sons, UK, pp 123-133 437 11. Ho, S. H., Huang, S. W., Chen, C. Y., Hasunuma, T., Kondo, A., & Chang, J. S. 438 Characterization and optimization of carbohydrate production from an indigenous 439 microalga Chlorella vulgaris FSP-E. Bioresource Technology, 2013, 135, 157-165. 440 12. John, R. P., Anisha, G. S., Nampoothiri, K. M., & Pandey, A. Micro and 441 macroalgal biomass: a renewable source for bioethanol. Bioresource technology, 2011, 442 102(1), 186-193. 443 13. López J.C., Quijano G., Souza T.S.O., Estrada J.M., Lebrero R., Muñoz R. 444 Biotechnologies for greenhouse gases (CH4, N2O, and CO2) abatement: state of the art 445 and challenges. Appl Microbiol Biotechnol, 2013, 97: 2277–2303. 446 14. Lowry, O., Rosenbrough, N., Farr, A., Randall, R., Protein measurement with 447 the folin phenol reagent. J. Biol. Chem. 1951, 193: 265−275. 448 15. Meier, L., Barros, P., Torres, A., Vilchez, C., Jeison, D. Photosynthetic biogas 449 upgrading using microalgae: Effect of light/dark photoperiod. Renewable Energy, 2017, 450 106, 17-23. 451 16. Mooij, P.R., Stouten, G.R.; Tamis, J.; van Loosdrecht, M.C.M., Kleerebezem R., 452 Survival of the fattest. Energy Environ. Sci., 2013, 6(12): 3404-3406. 453 20 17. Mooij, P.R., de Graaff, D.R., van Loosdrecht, M.C.M., Kleerebezem R., Starch 454 productivity in cyclically operated photobioreactors with marine microalgae—effect of 455 ammonium addition regime and volume exchange ratio. J Appl Phycol, 2015, 27: 1121. 456 18. Muñoz R., Meier L., Díaz I., Jeison D., A review on the state-of-the-art of 457 physical/chemical and biological technologies for biogas upgrading, Rev. Environ. Sci. 458 Biotechnol. 2015, 14(4): 727-759. 459 19. Park J.B.K., Craggs R.J., Wastewater treatment and algal production in high rate 460 algal ponds with carbon dioxide addition, Wat. Sci. Technol. 2010, 61: 633–639. 461 20. Posadas, E., Marín, D., Blanco, S., Lebrero, R., & Muñoz, R. Simultaneous 462 biogas upgrading and centrate treatment in an outdoors pilot scale high rate algal pond. 463 Bioresource Technology, 2017, 232, 133-141. 464 21. Posadas E., Morales M. M., Gómez C., Acién F. G., Muñoz R., Influence of pH 465 and CO2 source on the performance of microalgae-based secondary domestic 466 wastewater treatment in outdoors pilot raceways, Chem. Eng. J. 2015, 265: 239-248. 467 22. Raeesossadati M.J., Ahmadzadeh H., McHEnry M.P., Moheimani N.R. CO2 468 bioremediation by microalgae in photobioreactors: Impacts of biomass and CO2 469 concentrations, light, and temperature, Algal Res. 2014, 6: 78-85. 470 23. Raven, J. A., Beardall, J. 2003. Carbohydrate metabolism and respiration in 471 algae. In Photosynthesis in algae. pp. 205-224. Springer Netherlands. 472 24. Sander R. Compilation of Henry’s Law Constants for Inorganic and Organic 473 Species of Potential importance in Environmental Chemistry 1999. 474 25. Serejo, M.L., Posadas, E., Boncz, M.A., Blanco, S., García-Encina, P., Muñoz, 475 R., Influence of biogas flow rate on biomass composition during the optimization of 476 biogas upgrading in microalgal-bacterial processes. Environ. Sci. Technol. 2015, 49: 477 3228–3236. 478 21 26. Toledo-Cervantes A., Serejo M., Blanco S., Pérez R., Lebrero R., Muñoz R., 479 Photosynthetic biogas upgrading to bio-methane: boosting nutrient recovery via 480 biomass productivity control. Algal Res., 2016, 17: 56-52. 481 27. Toledo-Cervantes, A., Estrada, J. M., Lebrero, R., Muñoz, R. A comparative 482 analysis of biogas upgrading technologies: Photosynthetic vs physical/chemical 483 processes. Algal Res., 2017a. 25: 237-243. 484 28. Toledo-Cervantes, A., Madrid-Chirinos, C., Cantera, S., Lebrero, R., Muñoz, R. 485 Influence of the gas-liquid flow configuration in the absorption column on 486 photosynthetic biogas upgrading in algal-bacterial photobioreactors, Bioresour. 487 Technol, 2017b, 225: 336-342. 488 29. United Nations (2015) Climate change (Last access: March 2017): 489 http://www.cop21.gouv.fr/en/ 490 30. Warmuzinski K., Tanczyk M., Jaschik M., Experimental study on the capture of 491 CO2 from flue gas using adsorption combined with membrane separation, Int. J. 492 Greenh. Gas Con. 2015, 37: 182-190. 493 31. World Bank. 2014. World Development Indicators: Energy dependency, 494 efficiency and carbon dioxide emission, (Last access: March 2017): 495 http://wdi.worldbank.org/table/3.8 496 32. Zamalloa, C., Vulsteke, E., Albrecht, J., & Verstraete, W. The techno-economic 497 potential of renewable energy through the anaerobic digestion of microalgae. 498 Bioresource technology, 2011, 102(2), 1149-1158. 499 22 Figure captions 500 501 Figure 1. Schematic diagram of the experimental system used for the photosynthetic 502 CO2 removal from biogas and flue-gas. 503 Figure 2. Time course of a) the CO2 (○) and H2S (▲) removal efficiencies; and b) the 504 upgraded biogas composition CH4 (●), CO2 (■), N2 (□) and O2 (+). 505 Figure 3. Time course of the total nitrogen (TN) concentration in the cultivation broth. 506 Open circles represent the nitrogen concentration at the end of the dark period where the 507 nitrogen supplementation took place (8:00 am) and solid squares represent the nitrogen 508 concentration at the end of the illuminated period (8:00 pm). 509 Figure 4. Biomass concentration (■) and carbohydrates productivity (white bars) 510 achieved under different N-supplementation strategies. 511 Figure 4 Click here to download high resolution image Data Statement Click here to download Data Statement: dataprofile.xml