Energy production from microalgae biomass: carbon footprint and energy balance

Journal of Cleaner Production xxx (2014) 1e8

Contents lists available at ScienceDirect

Journal of Cleaner Production journal homepage: www.elsevier.com/locate/jclepro

Energy production from microalgae biomass: carbon footprint and energy balance Diego Lima Medeiros*, Emerson A. Sales, Asher Kiperstok ~o, Industrial Engineering Graduate Program (PEI) at Federal University of Bahia (UFBA), Escola Polit
ecnica, Rua Aristides Novis, n
2, 6
Andar e Federaça EP-UFBA, CEP 40.210-630, Salvador, BA, Brazil

a r t i c l e i n f o

a b s t r a c t

Article history: Received 22 September 2013 Received in revised form 16 May 2014 Accepted 15 July 2014 Available online xxx

Bioenergy sources are promising alternatives for sustainable energy production. Nevertheless, significant research and detailed analysis are necessary to identify the circumstances under which such energy sources can contribute to sustainability. This paper reviews the literature of Life Cycle Assessment (LCA) of microalgae-to-energy technologies and focuses in two categories, Greenhouse Gas (GHG) emissions and Net Energy Ratios (NER). The analysis is illustrated with a case study of microalgae biomass combustion to produce heat and compares the influence of different electricity sources with respect to GHG emissions and NER along the supply chain. Selected fossil energy sources were used as reference conditions. The methodology was LCA based on ISO 14044 standard, and most of the data used were extracted from a review of relevant scientific publications. Heat production from microalgae showed higher GHG emissions than those from fossil fuels with United States' electricity grid, but lower than those with the Brazilian one. The NER of heat from microalgae combustion life cycle is still disadvantageous compared to most of fossil options. However, the observation that fossil fuel options performed slightly better than microalgae combustion, in the two categories analyzed, must be understood in the context of a mature fossil energy technology chain. The fossil technology has less potential for improvements, while microalgae technology is beginning and has significant potential for additional innovations. © 2014 Elsevier Ltd. All rights reserved.

Keywords: Microalgae Nannochloropsis sp. Life cycle analysis Greenhouse gas Net Energy Ratio

1. Introduction The world relies on a continuous supply of energy to maintain the economic growth. The risk of an energy crisis may be reduced with more diversity of energy sources. Fossil fuels supply approximately 80% of the world's energy demand and are relatively inexpensive. However, the use of these fuels has added GHG to the atmosphere, thus contributing to global climate change. Biofuels are fuels derived from living matter, i.e. plants, animals, bacterias and fungi. Fossil fuels releases most of their GHG emissions in the combustion step while biofuels do from cultivation and processing steps (Zah et al., 2009). New technologies of biomass-toenergy conversion are currently in development and will play a decisive role in the world energy sector (Dovì et al., 2009). Microalgae-to-energy processes have being studied in recent decades, and industrial plants are currently being built to begin commercial generation of fuels from this source (Bahadar and Bilal

* Corresponding author. Tel.: þ55 71 3283 9800; fax: þ55 71 3283 9801. E-mail address: [email protected] (D.L. Medeiros).

Khan, 2013). On the other hand, Davis et al. (2011) declared that the near-term economic viability of algal biofuels is uncertain due to speculation surrounding the processes of scaling-up this emerging industry. Some researches are interested in analyzing the NER and GHG emissions of microalgae-to-energy technologies (Lam and Lee, 2012; Lam et al., 2012). The reason is that methods, to grow and process algae, vary according to the location, species of algae being grown, and the products intended to be taken. This paper reviews some of the latest discoveries in this field and explores a simulated case study.

2. Microalgae-to-energy 2.1. Cultivation The first step in algal bioenergy production, the microalgae biomass growth, is often a decisive step, as it demands most of the inputs in the entire process chain. A comparative assessment of microalgae cultivation was conducted to characterize the range of

http://dx.doi.org/10.1016/j.jclepro.2014.07.038 0959-6526/© 2014 Elsevier Ltd. All rights reserved.

Please cite this article in press as: Medeiros, D.L., et al., Energy production from microalgae biomass: carbon footprint and energy balance, Journal of Cleaner Production (2014), http://dx.doi.org/10.1016/j.jclepro.2014.07.038

2

D.L. Medeiros et al. / Journal of Cleaner Production xxx (2014) 1e8

inputs required in this step for open and closed systems, Tables 1 and 2 respectively. The data varies significantly between authors. Uncertainty in energy inputs at cultivation affects the NER and consequently the GHG emissions (Rogers et al., 2013). Handler et al. (2012) did a similar comparison between LCA studies and found variations in energy use at cultivation step of two orders of magnitude. Further comments on these tables are in the discussion section. 2.2. Scaling up of microalgae production Significant improvements to reduce the infrastructure and operational costs, in order to scale-up microalgae production chain, must be performed to produce commercially viable products from
rez-Lo
pez et al. (2013a,b) found the usage of commicroalgae. Pe mercial fertilizer and electricity as the major contributors to the environmental impacts of microalgae products. A defined set of technology breakthroughs will be required to optimize the production of microalgae biofuels at scale (Singh and Olsen, 2011; Um and Kim, 2009). Table 3 summarizes most of the current challenges and opportunities related to commercial exploitation of algal biofuels. Biofuels based on algal biomass may play a decisive role in future energy production chains if technological breakthroughs can address challenges mentioned in Table 3. Koller et al. (2012) state the possibility of mixotrophic cultivation of microalgae, combining removal of pollutants from wastewater in a heterotrophic phase and production of high added value products in an autotrophic phase. Therefore, the carbon dioxide input required to nourish the microalgae growth can be supplied from low cost sources such as flue gases from boilers, furnaces or power plants (Sander and Murthy, 2010; Campbell et al., 2010). In addition, combustion products such as nitrogen oxides and sulfur oxides can be effectively used by microalgae as nutrients (Um and Kim, 2009; Packer, 2009; Yoo et al., 2010). Also, most of the nutrients needed for algal growth, except carbon, may be obtained from municipal wastewater with the function of nutrient removal (Yang et al., 2011; U.S. DOE, 2010; Park et al., 2011; Pittman et al., 2011; Itoiz et al., 2012;

Olguín, 2012; Fenton and OhUallach ain, 2012). In Table 4 are presented the conclusions of selected literature related to energy balance of different microalgae biofuels. The studies in Table 4 found both, favorable and unfavorable, energy balances over the biofuel life cycle depending on the technological scenario modeled. According to Singh and Olsen (2011) it is difficult to identify preferred routes of biofuel production from algal biomass at the current stage of development. Holma et al. (2013) affirm the results of the microalgae production chain are

uncertain due to the early development stage of the technology and the assumptions made concerning the electricity grid, which can vary significantly between different sites. Clarens et al. (2011) compared three different routes of energy production from microalgae biomass for transportation purposes, such as: combined biodiesel and electricity production from biogas, combined biodiesel and electricity production from biomass combustion, and electricity production from biomass combustion alone. The authors identified the most advantageous NER came from the third route. Some studies concluded that microalgae lipid extraction is an energy intensive process (Clarens et al., 2011;
rez-Lo
pez et al., 2013a). Pe 3. Methods The case study aimed to evaluate the environmental and energetic performance of thermal recovery from biomass combustion using microalgae cultivated in Open Ponds (OP) and Flat Plate Photobioreactors (FPP). We modeled the GHG emissions and NER over the life cycle and compared them with selected fossil sources. Most of the data used in this analysis came from scientific literature, as the authors were not aware of any commercial industrial plant producing bioenergy photosynthetically from microalgae as of the writing of this article. 3.1. Goal and scope definition This study was based on the methodology of Life Cycle Assessment (LCA) according to ISO 14044 (2006). Each production chain considered two scenarios for cultivation: OP1 e algal biomass, open pond, flue gas. OP2 e algal biomass, open pond, flue gas and wastewater. FPP1 e algal biomass, flat plate, flue gas. FPP2 e algal biomass, flat plate, flue gas and wastewater. The cut-off rule was applied to waste streams, flue gas and wastewater. This assumption means that treatment gains or environmental loads from waste streams production were not recorded. Scenarios OP1 and FPP1 were supplied by tailing water from desalination, as the algae genus used was Nannochloropsis, a microalgae originally from the sea. Scenarios OP2 and FPP2 used two sources of water, tailing water from desalination and wastewater as a nutrient source. This practice has been found to replace the use of chemical fertilizers without any productivity loss (Yang et al., 2011; Jiang et al., 2011; Perelo et al., 2012).

Table 1 Inputs in open pond microalgae cultivation per kilogram of produced dry biomass. Method

Open ponds

Authors

Chisti, 2007.

Species

Chlorella Chlorella vulgaris, Chlorella vulgaris, Nannochloropsis Dunaliella vulgaris normal less N sp.

Process parameters Energy CO2 N P Water Growth

Unit

kWh kg kg kg m3 g/m2 day Concentration kg/m3 Oil content %

Lardon et al., 2009.

Lardon et al., 2009.

Jorquera et al., 2010

Campbell Clarens et al., Stephenson Quinn et al., 2010. 2010. et al., 2010. et al., 2011

Razon and Tan, 2011.

Mix of microalgae

Chlorella vulgaris

Nannochloropsis Nannochloropsis oculata sp.

Quantity

e 1.83 0.07 0.01 7.1 e

0.35 1.75 0.046 e e 25

0.42 1.97 0.01 e e 19

1.05 e e e 2.8 11

0.2 1.69 0.008 0.0056 0.7 30

0.19 e e e e 15

0.8 e 0.024 e 0.7 30

e e e e e 15

12.7 e 0.007 0.013 e 16

0.1 30

0.5 18

0.5 40

0.35 30

e e

1 e

1.67 40

3 51

0.13 30

Please cite this article in press as: Medeiros, D.L., et al., Energy production from microalgae biomass: carbon footprint and energy balance, Journal of Cleaner Production (2014), http://dx.doi.org/10.1016/j.jclepro.2014.07.038

D.L. Medeiros et al. / Journal of Cleaner Production xxx (2014) 1e8

3

Table 2 Inputs in photobioreactors microalgae cultivation per kilogram of produced dry biomass. Method

Tubular

Flat-plate

Polyethylene bags

Hybrid, FPP and OP

Author

Chisti, 2007.

Collet et al., 2011.

Stephenson et al., 2010.

Jorquera et al., 2010

Batan et al., 2010.

Khoo et al., 2011

Razon and Tan, 2011.

Species

Chlorella vulgaris

Chlorella vulgaris

Chlorella vulgaris

Nannochloropsis sp.

Nannochloropsis salina

Nannochloropsis sp.

Haematococcus pluvialis

Process parameters

Unit

Quantity

Energy CO2 N P Water Growth

kWh kg kg kg m3 g/m2 day kg/m3 %

e 1.83 0.07 0.01 0.25 e

0.23 1.17 0.01 0.002 e 25

7.27 e 0.0236 e 0.134 75

1.94 e e e 0.37 27

0.455 e 0.147 0.02 0.134 25

0.972 1.83 0.15 0.01 2125 e

5.77 e 0.0128 0.013 e 16

4 30

0.5 e

8.3 40

2.7 30

e e

0.5 e

0.43 25

Concentration Oil content

3.2. Inventory The reference flow adopted was 1 kg of biomass with a Lower Heating Value (LHV) of 18.26 Mega Joules (MJ), calculated for Nannochloropsis biomass in Appendix I. The functional unit for comparison with fossil fuels was 20 MJ of LHV. The infrastructure materials for the cultivation and harvesting step were neglected in these calculations, as the impact was assumed to be negligible over the lifespan of the building (Grierson et al., 2013). The following assumptions were used for the definition of the system model: 3.2.1. Cultivation The electricity consumption in the cultivation stage is primarily due to flue gas pressurization and pumping into the culture medium, water pumping for recirculation, and water pumping for cooling in the FPP scenarios (Jorquera et al., 2010). The electricity sources used were the medium voltage electricity grid from United States (U.S.) and Brazil (BR) from Ecoinvent (2013). The flue gas and wastewater were assumed to be located close to the microalgae farms, thus needing no further transport requirements as Rickman et al. (2013) point. The water may come from the sea or saline aquifers, which are common in the semiarid region of Brazil and showed a favorable growth medium for Nannochloropsis in combination with wastewater after secondary treatment (Perelo et al., 2012; Jiang et al., 2011). The reason to choose this algae was the capacity to cultivate it in OP without using pesticides, as the salt water may inhibt predors. The water evaporation losses in the OP systems were neglected, as all of the water used was previously wastewater. The OP1 and FPP1 scenarios used commercial fertilizers manufactured in Europe. The biomass concentrations at the point of harvest were 0.35 kg/ m3 in OP and 2.7 kg/m3 in FPP according to Jorquera et al. (2010), and the maximum algae concentration is achieved with a growth period of 7 days. These data were used to estimate the volume of cultivation medium needed for each kilogram of microalgae biomass harvested. 3.2.2. Harvesting It was considered three harvesting steps (flocculation, decantation and centrifugation) and a drying stage (solar-greenhouse) to set the biomass suitable for energy recovery through combustion to generate heat. The products used in flocculation process were assumed to be produced in Europe. Weschler et al. (2014) identified thermal drying as an undesirable process, it offsets most of possible GHG and NER gains. The solar-greenhouse does not require any

significant direct input other than sunlight, reason why this step was neglected from the inventory. 3.2.3. Combustion There is lack of data on microalgal biomass combustion process. The inventory of a thermoelectric power plant fueled by perishable household waste was selected as a representative inventory for microalgal biomass combustion from Ecoinvent (2013). 4. Results 4.1. Inventory Table 5 presents the inventory of Nannochloropsis sp. dry biomass production used to analyse the GHG emissions and NER. More analysis of the inventory, Table 5, are in the discussion section. 4.2. Greenhouse Gases (GHG) Fig. 1 presents the GHG emissions of the production chains, OP1, OP2, FPP1 and FPP2, and selected fossil fuel options obtained from the Ecoinvent (2013) as follows: Heat, at hard coal industrial furnace 1-10 MW/RER1; Heat natural gas, at industrial furnace > 100 kW/ RER1; Heat, heavy fuel oil, at industrial furnace 1 MW/RER1; Heat, light fuel oil, at industrial furnace 1 MW/RER.1 The GHG emissions from microalgae scenarios varied significantly, with cases better than most fossil fuel options as BR OP2 or worse like U.S. FPP1. In Fig. 2 is shown the GHG contribution of U.S. OP1 production chain. The production chains of the other microalgae scenarios are similar. It is noticeable that the processes which contributed most to GHG emissions were N fertilizer, electricity and aluminium sulphate with 16%, 37% and 28% respectively. More analysis of these results, Figs. 2 and 3, are hereafter in the next subsection. 4.3. Net Energy Ratio (NER) The energy balance or NER was calculated as the energy contained in the final product, the output energy (E Out) of the system, divided by the Cumulative Energy Demand (CED) along the

1

The acronym RER means Europe Region.

Please cite this article in press as: Medeiros, D.L., et al., Energy production from microalgae biomass: carbon footprint and energy balance, Journal of Cleaner Production (2014), http://dx.doi.org/10.1016/j.jclepro.2014.07.038

4

D.L. Medeiros et al. / Journal of Cleaner Production xxx (2014) 1e8

Table 3 Challenges to commercial-scale implementation of microalgae-to-biofuel schemes. Cultivation

Opportunities

Obstacles

CO2 Nutrients Water Infrastructure and Operation Sun/light

Available at low cost from energy-intensive industrial plantsa Available at low cost from secondary wastewater treatment plants Can be recirculated Offer more control to the processes

Land shortage around these industrial areasb Not well studied yetc This practice is not well established yetd High cost and currently is intensive in energye

Arid areas are one promising source

Temperature

Harvesting

Sites surrounding mountains, rainforests, or large water bodies often have temperatures amenable to production Several wild types of algae have been used without selection or modification Starve algae from nitrogen increase lipid's productivityj Microalgae from lab did not stand under robust conditions encountered in the field There are many technologies being used and in development

The resources should be transported through long distances and it needs investment in infrastructure Normally these places are protected. In arid areas temperature control may impose a challengef The algae will have to be domesticatedh

Lipid extraction Biomass

There are promising technologies being developed It can be converted in many forms of biofuels.

Species Oil productivity Contamination

a b c d e f g h i j

Slow down growth yield and consequently operation costs Allow a contaminant native to the area take over the pondsf It has to be adapted for a specific specie, medium and downstream processg It will depend on the specie of algae and how it was grownh Not all of them have being successful tested in pilot scale yeti

Campbell et al. (2010). Pate et al. (2011). Park et al. (2011); Christenson and Sims (2011). Yang et al. (2011). Norsker et al. (2011). Sheehan et al. (1998). Uduman et al. (2010); Mata et al. (2010); Udom et al. (2013). Rawat et al. (2011); Benemann (2010). Singh and Olsen (2011). Lardon et al. (2009).

production chain, the input energy (E In) of the system (Delrue et al., 2012; Zhang and Colosi, 2013). The results are shown in Fig. 3.

.X NER ¼ E Out E In

(1)

The OP2 and FPP2 scenarios performed more favorable results than the OP1 and FPP1 scenarios in both categories assessed, GHG and NER, due to the elimination of commercial fertilizers, which require significant energy inputs for their production and transportation, while wastewater contains the same nutrients “for free”. Table 4 Comparison of energy balances for microalgae biofuel production over the life cycle. Studies

Description

NER  1

Lardon et al. (2009)

Biodiesel production from microalgae Biomass production from microalgae Methanol production from microalgae Biodiesel production from microalgae Biomass production using different methods Biodiesel produced from six microalgae (raceway) models Biodiesel and methane produced from microalgae Biodiesel production from microalgae Biodiesel and Biogas production from microalgae Biodiesel production from microalgae Biodiesel and Biogas production from microalgae Biooil and Biogas production from microalgae Biodiesel production from microalgae

X

Clarens et al. (2010) Liu and Ma (2009) Scott et al. (2010) Jorquera et al. (2010) Liu et al. (2011)

Razon and Tan (2011) Itoiz et al. (2012) Delrue et al. (2012) Delrue et al. (2013) Quinn et al. (2013) Khoo et al. (2013) Passell et al. (2013)

NER < 1 Table 5 Global inventory for the production of 1 kg (dry matter) of Nannochloropsis biomass in Open-ponds (OP) and Flat-plate photobioreactors (FPP).

X

Process parameters

X X X

X

X

X

X X X

The substitution of reclaimed wastewater for commercial fertilizers reduced the GHG emissions by 22% U.S. OP, U.S. FPP 16%, BR OP 35%, BR FPP 33% and increased the NER by 24% U.S. OP, U.S. FPP 19%, BR OP 34%, BR FPP 29%. Nevertheless, the emissions associated with microalgae production and combustion are not significantly different from those of most fossil fuels, due to the significant uncertainties associated with both fuel sources. It is noteworthy that electricity from the U.S. grid, which is predominantly derived from fossil fuels, is more GHG intensive and less efficient in the energy conversion compared to the Brazilian one. It was identified in the Ecoinvent (2013) with the method CED that each MJ of electricity from the medium voltage electrical grid demands 3.55 MJ in US and 1.4 MJ in BR. The reason is that

X

X

Cultivation Nitrogen (N) Phosphorus (P) Potassium (K) Fertilizers transportation Carbon dioxide (CO2) Water Electricity Microalgae þ Water Floculation Aluminum Sulfate Al2(SO4)3 Hydrochloric Acid HCL (15%)

X

X

X

X X

Flocculent transportation Microalgae þ moisture Centrifugation Electricity

OP

FPP

Unit

Source

0.07 0.01 0.01 0.02 1.83 2857.14

0.07 0.01 0.01 0.02 1.83 370.37

kg/kg kg/kg kg/kg t.km kg/kg kg/kg

1.05

1.94

This study This study This study Estimated Chisti 2007 Jorquera et al., 2010 Jorquera et al., 2010

2858.14

371.37

kg/kg

1.3

1.3

kg/kg

0.3

0.3

kg/kg

0.16 8

0.16 1.04

t km kg/kg

0.06

0.001

kWh/kg

kWh/kg

Razon and Tan, 2011 Razon and Tan, 2011 Estimated Calculated Brentner et al., 2011

Please cite this article in press as: Medeiros, D.L., et al., Energy production from microalgae biomass: carbon footprint and energy balance, Journal of Cleaner Production (2014), http://dx.doi.org/10.1016/j.jclepro.2014.07.038

D.L. Medeiros et al. / Journal of Cleaner Production xxx (2014) 1e8

5

Fig. 1. GHG emissions of 20 MJ LHV from Nannochloropsis under scenarios OP1, OP2, FPP1 and FPP2 as compared to representative fossil fuels. Source: method IPCC (2007) GWP 100a.

hydroelectricity is less GHG intensive and more efficient than thermoelectricity from fossil fuels. The influence of the electricity input in the outcomes of the different scenarios in the cultivation step were identified. The GHG emissions for BR scenarios for OP1, OP2, FPP1 and FPP2 decreased by 32%, 38%, 42% and 50% respectively, while their NER improved 28%, 36%, 42% and 55% respectively, in comparison to the US scenarios. Inputs such as fertilizers and flocculants were assumed to retain their original electrical grid from Europe, as most of these products are typically imported. In the cultivation step under scenarios OP1 and FPP1, the use of electricity and fertilizers accounted for the greatest contributions to GHG emissions (Fig. 2). The largest contribution among the different fertilizers used was the nitrogenous fertilizer. In scenarios OP2 and FPP2, with no commercial fertilizers used, electricity input was the major source of GHG emissions of the production chain. In the harvesting step the aluminum sulfate flocculent used was the major

source of GHG emissions due to the high electricity consumption required for the production of this input, presumably from the European electrical grid, with its predominant fossil fuel matrix. 5. Discussion The literature review showed that electricity is a key input in the cultivation of microalgae due to pumping of flue gases and water in the culture medium. In disagreement with the findings of Clarens et al. (2011) we found that the cultivation of microalgae biomass for combustion and thermal recovery is not viable from an energy balance perspective, NER<1. Surprisingly, the fossil fuel options also proved to be unviable despite the significant uncertainty ranges of the results (Fig. 3). Several optimization opportunities exist in microalgae-toenergy production chain to reduce the environmental impacts and costs, such as those shown in Table 3. Even though microalgae

Fig. 2. GHG contribution along the production chain of heat production from Nannochloropsis under scenario U.S. OP1. Source: SimaPro 8 ®.

Please cite this article in press as: Medeiros, D.L., et al., Energy production from microalgae biomass: carbon footprint and energy balance, Journal of Cleaner Production (2014), http://dx.doi.org/10.1016/j.jclepro.2014.07.038

6

D.L. Medeiros et al. / Journal of Cleaner Production xxx (2014) 1e8

Fig. 3. NER of 20 MJ LHV from Nannochloropsis under scenarios OP1, OP2, FPP1 and FPP2 as compared to representative fossil fuels. Source: method CED, Jungbluth and Frischknecht (2007).

biomass is not yet an established alternative fuel source for energy production. Studies like the current one and those ones in Table 4 are valuable in directing further efforts to develop and implement economically viable and environmentally sustainable microalgaeto-energy technologies. Key differences in the input and output parameters can be observed comparing the data from literature studies reviewed in Tables 1 and 2 with the present case study. For example, the consumption of electricity per kg of microalgae dry biomass in OP cultivation step of the present study was 1.05 kWh, while, despite the use of different species of microalgae, most authors' estimates ranged from 0.19 to 0.42 kWh, with the exception of Stephenson et al. (2010) and Razon and Tan (2011). Using these most common literature values for this parameter would reduce the electricity inputs for this step by 60e80%. Such a substitution would result in an even greater difference in FPP cultivation step, as the current study used an electricity consumption of 1.94 kWh per kg of dry microalgae, whereas most authors have published values ranging from 0.3 to 0.94 kWh, again with the exception of Stephenson et al. (2010) and Razon and Tan (2011). These differences represent a potential reduction of 52%e85% in electricity consumption. A possible 70% reduction in electricity consumption at the cultivation stage under the best U.S. scenario analysed, U.S. OP2, would reduce the estimated GHG by approximately 42%, resulting in an emission of 0.85 kg CO2e per 20 MJ LHV. This change would make this scenario appear more favorable in comparison with any fossil fuel options. Regarding the NER, applying the same reduction in electricity consumption for U.S. OP2 scenario would constitute a technological breaking even point, when NER equals 1. In this case, the microalgae production chain would be able to supply its whole demand along the life cycle and lower GHG emissions close to zero. This is because U.S. scenarios have most of the energy inputs coming from fossil fuels. A scenario of microalgae-to-energy with NER > 1 would be able to supply the entire production chain, producing real gains and reducing GHG emissions considerably. This simulation demonstrates how the microalgae-to-energy technology could become economically viable and environmentally sustainable. There is little room to reduce GHG emissions along the fossil fuel production chain, as most of these emissions happen in the combustion step, and the current technology is mature. Moreover, the costs and emissions associated with extracting fossil energy sources are likely to increase as these fuel sources become scarcer. By contrast, microalgae combustion has significantly lower GHG emissions, due to the fact that the GHG emitted at this stage is considered renewable. Therefore, microalgae bioenergy technologies offer greater opportunities to minimize GHG emissions along the supply chain in the near future.

6. Conclusion The results of this paper confirm the potential of microalgae biomass as an energy source, but demonstrate the need to decrease the use of electricity, fertilizers and other inputs, such as chemical flocculants. The starting point for the economic and environmental viability of energy production from microalgae biomass is the achievement of a favorable energy balance, NER  1. This study demonstrates that the use of flue gas, residual nutrients from wastewater and cleaner electricity grids enables significant reductions in GHG emissions and improvements in the energy balance associated with microalgae-to-energy. The influence of country electricity grids to GHG emissions and NER over the microalgae life cycle analysis was decisive when compared to fossil fuels. These actions increase the opportunities for competitive commercialization of microalgae energy products. The fact that the Brazilian energy matrix is less GHG intensive and more efficient in NER compared to the world average places the country in a better position to promote the production of algal biomass as a renewable energy source. Topics that should be explored further in future research include the assessment of other routes for biofuel production such as biodiesel, biomethane and bioethanol, local productivity rates, comparison with other renewable energy sources, and the evaluation of other environmental LCA categories like land use impacts, resources depletion and eutrofization. Acknowledgments This research study was supported by the program Institutos ^ncia e Tecnologia (INCT) of the Conselho Nacional Nacionais de Cie
gico (CNPq/MCT) and de Desenvolvimento Científico e Tecnolo ~o de Aperfeiçoamento de Pessoal de Nível Superior Coordenaça (CAPES) for their research scholarships, the Ecoinvent for the internship supervised by Mireille Faist, and the company ACVBrasil
Consultants for concession of the educational lion behalf of Pre cense for Simapro with Ecoinvent database. Appendix A The calculation of the Lower Heating Value (LHV) was based on the cellular composition of microalgae biomass, CO0,48H1,83N0,11P0,01, given by Grobbelaar (2004 apud Chisti, 2007). The stoichiometric balance of combustion is CO0,48H1,83N0,11P0,01 þ 2O2 / 1CO2 þ 0.91H2O þ 0.11NO2 We neglected the contribution of P in the stoichiometric balance. The water vaporization enthalpy (DHvapH2O) at 20
C was taken as 44.016 kJ/g mol. See the calculation table of LHV from Nannochloropsis sp., Table A.1.

Please cite this article in press as: Medeiros, D.L., et al., Energy production from microalgae biomass: carbon footprint and energy balance, Journal of Cleaner Production (2014), http://dx.doi.org/10.1016/j.jclepro.2014.07.038

D.L. Medeiros et al. / Journal of Cleaner Production xxx (2014) 1e8

Atomic weight Microalgae biomass molecular composition Multiplication Sum

7

C

O

H

N

Comments

12 1

16 0.48

1 1.83

14 0.11

Grobbelaar 2004 apud Chisti 2007

12 23.05 1000 g or 1 kg Number of g mols of biomass Higher Heating Value (HHV) 1 g mol of biomass Vaporization enthalpy of H2O

7.68 g/g mol

1.83

1.54

43.38

1 Kg of biomass or Lower Heating Value (LHV) LHV/HHV or 1 LHV equivalent to

Lines 1 2

Line 1 items  Line 2 items Result of Line 3 operation

3 4 5

g mols

Line 5/Line 4

6

20

MJ/kg

Sforza et al., 2011

7

0.91

g mol H2O

8

44.02

kJ/g mol

9

40.05 1737.72 1.73 18.26 0.91 1.10

kJ kJ MJ MJ/kg

References Bahadar, A., Bilal Khan, M., 2013. Progress in energy from microalgae: a review. Renew. Sustain. Energy Rev. 27, 128e148. http://dx.doi.org/10.1016/ j.rser.2013.06.029. Benemann, J., 2010. AIM Interview: Dr. John Benemann by David Schwartz. Algae Industry Magazine. Available at: http://www.algaeindustrymagazine.com/theaim-interview-dr-john-benemann/. Batan, L., Jason, Q., Bryan, W., Thomas, B., 2010. Net energy and greenhouse gas emission evaluation of biodiesel derived from microalgae. Environ. Sci. Technol. 44 (20), 7975e7980. http://www.ncbi.nlm.nih.gov/pubmed/20866061. Brentner, L.B., Eckelman, M.J., Zimmerman, J.B., 2011. Combinatorial life cycle assessment to inform process design of industrial production of algal biodiesel. Environ. Sci. Technol. 45 (16), 7060e7067. http://dx.doi.org/10.1021/es2006995. Campbell, P.K., Beer, T., Batten, D., 2010. Life cycle assessment of biodiesel production from microalgae in ponds. Bioresour. Technol. http://dx.doi.org/ 10.1016/j.biortech.2010.06.048. Chisti, Y., 2007. Biodiesel from microalgae. Biotechnol. Adv. 25 (3), 294e306. http:// dx.doi.org/10.1016/j.biotechadv.2007.02.001. Christenson, L., Sims, R., 2011. Production and harvesting of microalgae for wastewater treatment, biofuels, and bioproducts. Biotechnol. Adv. 29 (6), 686e702. http://dx.doi.org/10.1016/j.biotechadv.2011.05.015. Clarens, A.F., et al., 2011. Environmental impacts of algae-derived biodiesel and bioelectricity for transportation. Environ. Sci. Technol. 45, 7554e7560. Clarens, A.F., Resurreccion, E.P., White, M.A., Colosi, L.M., 2010. Environmental life cycle comparison of algae to other bioenergy feedstocks. Environ. Sci. Technol. 44 (5), 1813e1819. http://dx.doi.org/10.1021/es902838.
lias, A., Lardon, L., et al., 2011. Life-cycle assessment of microalgae Collet, P., He culture coupled to biogas production. Biores. Technol. 102, 207e214. http://dx. doi.org/10.1016/j.biortech.2010.06.154. Davis, R., Aden, A., Pienkos, P.T., 2011. Techno-economic analysis of autotrophic microalgae for fuel production. Appl. Energy 88 (10), 3524e3531. http:// dx.doi.org/10.1016/j.apenergy.2011.04.018. Delrue, F., Li-Beisson, Y., Setier, P., et al., 2013. Comparison of various microalgae liquid biofuel production pathways based on energetic, economic and environmental criteria. Bioresour. Technol. 136, 205e212. http://dx.doi.org/10.1016/ j.biortech.2013.02.091. Delrue, F., Setier, P., Sahut, C., et al., 2012. An economic, sustainability, and energetic model of biodiesel production from microalgae. Bioresour. Technol. 111, 191e200. http://dx.doi.org/10.1016/j.biortech.2012.02.020. Dovì, V.G., Friedler, F., Huisingh, D., Klemes, J.J., 2009. Cleaner energy for sustainable future. J. Clean. Prod. 17 (10), 889e895. http://dx.doi.org/10.1016/ j.jclepro.2009.02.001. Ecoinvent v2.2, 2013. Life Cycle Inventory Database. Available at: www.ecoinvent. org.
Uallach
Fenton, O., Oh ain, D., 2012. Agricultural nutrient surpluses as potential input sources to grow third generation biomass (microalgae): a review. Algal Res. 1 (1), 49e56. http://dx.doi.org/10.1016/j.algal.2012.03.003. Grierson, S., Strezov, V., Bengtsson, J., 2013. Life cycle assessment of a microalgae biomass cultivation, bio-oil extraction and pyrolysis processing regime. Algal Res. 2 (3), 299e311. http://dx.doi.org/10.1016/j.algal.2013.04.004. Handler, R.M., Canter, C.E., Kalnes, T.N., et al., 2012. Evaluation of environmental impacts from microalgae cultivation in open-air raceway ponds: analysis of the

HHV

Line 8  Line 9 Line 10  Line 6 Line 7 e Line 12 Line 13/Line 7 1/Line 14

10 11 12 13 14 15

prior literature and investigation of wide variance in predicted impacts. Algal Res. 1 (1), 83e92. http://dx.doi.org/10.1016/j.algal.2012.02.003. Holma, A., Koponen, K., Antikainen, R., Lardon, L., Leskinen, P., Roux, P., 2013. Current limits of life cycle assessment framework in evaluating environmental sustainability e case of two evolving biofuel technologies. J. Clean. Prod. 54, 215e228. http://dx.doi.org/10.1016/j.jclepro.2013.04.032. ISO 14044, 2006. International Standard. Environmental Management e Life Cycle Assessment e Requirements and Guidelines. International Organization for Standardization, Geneva, Switzerland. Itoiz, E.S., Fuentes-Grünewald, C., Gasol, C.M., et al., 2012. Energy balance and environmental impact analysis of marine microalgal biomass production for biodiesel generation in a photobioreactor pilot plant. Biomass Bioenergy 39, 324e335. http://dx.doi.org/10.1016/j.biombioe.2012.01.026. Jiang, L., Luo, S., Fan, X., Yang, Z., Guo, R., 2011. Biomass and lipid production of marine microalgae using municipal wastewater and high concentration of CO2. Appl. Energy 88 (10), 3336e3341. http://dx.doi.org/10.1016/ j.apenergy.2011.03.043. Jorquera, O., Kiperstok, A., Sales, E.A., Embiruçu, M., Ghirardi, M.L., 2010. Comparative energy life-cycle analyses of microalgal biomass production in open ponds and photobioreactors. Bioresour. Technol. 101 (4), 1406e1413. http://dx.doi.org/ 10.1016/j.biortech.2009.09.038. Jungbluth, N., Frischknecht, R., 2007. Part II, 2 cumulative energy demand. ecoinvent report No. 3, v2.0. In: Frischknecht, R., Jungbluth, N., Althaus, H.-J., et al. (Eds.), Implementation of Life Cycle Impact Assessment Methods. Swiss Centre for Life Cycle Inventories, Dübendorf. Khoo, H.H., Koh, C.Y., Shaik, M.S., et al., 2013. Bioenergy co-products derived from microalgae biomass via thermochemical conversionelife cycle energy balances and CO2 emissions. Bioresour. Technol. 143, 298e307. http://dx.doi.org/10.1016/ j.biortech.2013.06.004. Khoo, H.H., Sharratt, P.N., Das, P., et al., 2011. Life cycle energy and CO2 analysis of microalgae-to-biodiesel: preliminary results and comparisons. Biores. Technol. http://dx.doi.org/10.1016/j.biortech.2011.02.055. €chzelt, H., Schober, S., Braunegg, G., Koller, M., Salerno, A., Tuffner, P., Koinigg, M., Bo 2012. Characteristics and potential of micro algal cultivation strategies: a review. J. Clean. Prod. 37, 377e388. http://dx.doi.org/10.1016/j.jclepro.2012.07.044. Lam, M.K., Lee, K.T., 2012. Microalgae biofuels: a critical review of issues, problems and the way forward. Biotechnol. Adv. 30 (3), 673e690. http://dx.doi.org/ 10.1016/j.biotechadv.2011.11.008. Lam, M.K., Lee, K.T., Mohamed, A.R., 2012. Current status and challenges on microalgae-based carbon capture. Int. J. Greenh. Gas Control 10, 456e469. http://dx.doi.org/10.1016/j.ijggc.2012.07.010.
lias, A., Sialve, B., Steyer, J.P., Bernard, O., 2009. Life-cycle assessment of Lardon, L., He biodiesel production from microalgae. Environ. Sci. Technol. 43 (17), 6475e6481. http://dx.doi.org/10.1021/es900705j. American Chemical Society. Liu, J., Ma, X., 2009. The analysis on energy and environmental impacts of microalgae-based fuel methanol in China. Energy Policy 37 (4), 1479e1488. Liu, X., Clarens, A.F., Colosi, L.M., 2011. Algae biodiesel has potential despite inconclusive results to date. Bioresour. Technol. http://dx.doi.org/10.1016/ j.biortech.2011.10.077. Mata, T.M., Martins, A.A., Caetano, N.S., 2010. Microalgae for biodiesel production and other applications: a review. Renew. Sustain. Energy Rev. 14, 217e232. €, M.H., Wijffels, R.H., 2011. Microalgal producNorsker, N.H., Barbosa, M.J., Vermue tion e a close look at the economics. Biotechnol. Adv. 29 (1), 24e27. http:// dx.doi.org/10.1016/j.biotechadv.2010.08.005.

Please cite this article in press as: Medeiros, D.L., et al., Energy production from microalgae biomass: carbon footprint and energy balance, Journal of Cleaner Production (2014), http://dx.doi.org/10.1016/j.jclepro.2014.07.038

8

D.L. Medeiros et al. / Journal of Cleaner Production xxx (2014) 1e8

Olguín, E.J., 2012. Dual purpose microalgae-bacteria-based systems that treat wastewater and produce biodiesel and chemical products within a biorefinery. Biotechnol. Adv. 30 (5), 1031e1046. http://dx.doi.org/10.1016/ j.biotechadv.2012.05.001. Packer, M., 2009. Algal capture of carbon dioxide: biomass generation as a tool for greenhouse gas mitigation with reference to New Zealand energy strategy and policy. Energy Pol. 37 (9), 3428e3437. http://dx.doi.org/10.1016/j.enpol.2008.12. 025. Park, J.B.K., Craggs, R.J., Shilton, A.N., 2011. Wastewater treatment high rate algal ponds for biofuel production. Bioresour. Technol. 102 (1), 35e42. http:// dx.doi.org/10.1016/j.biortech.2010.06.158. Passell, H., Dhaliwal, H., Reno, M., et al., 2013. Algae biodiesel life cycle assessment using current commercial data. J. Environ. Manag. 129, 103e111. http:// dx.doi.org/10.1016/j.jenvman.2013.06.055. Pate, R., Klise, G., Wu, B., 2011. Resource demand implications for US algae biofuels production scale-up. Appl. Energy 88 (10), 3377e3388. http://dx.doi.org/ 10.1016/j.apenergy.2011.04.023. Perelo, L.W., Sousa, L.L., Hora, D.S., 2012. Crescimento da microalga Nannochloropsis ~o de esgoto domestico como fonte sp. em
agua salina do semi-
arido com adiça de nutrientes. II Congresso Baiano de Engenharia Sanit
aria e Ambiental, Feira de Santana e BA, Brazil.
rez-Lo
pez, P., Gonza
lez-García, S., Ulloa, R.G., Sineiro, J., Feijoo, G., Moreira, M.T., Pe 2013a. Life cycle assessment of the production of bioactive compounds from Tetraselmis suecica at pilot scale. J. Clean. Prod., 1e9. http://dx.doi.org/10.1016/ j.jclepro.2013.07.028.
rez-Lo
pez, P., Gonza
lez-García, S., Jeffryes, C., Agathos, S.N., McHugh, E., Walsh, D., Pe Moreira, M.T., 2013b. Life cycle assessment of the production of the red antioxidant carotenoid astaxanthin by microalgae: from lab to pilot scale. J. Clean. Prod. http://dx.doi.org/10.1016/j.jclepro.2013.07.011. Pittman, J.K., Dean, A.P., Osundeko, O., 2011. The potential of sustainable algal biofuel production using wastewater resources. Biores. Technol. 102 (1), 17e25. http://dx.doi.org/10.1016/j.biortech.2010.06.035. Quinn, J.C., Smith, T.G., Downes, C.M., et al., 2013. Microalgae to biofuels lifecycle assessment d Multiple pathway evaluation. Algal Res., 1e7. http://dx.doi.org/ 10.1016/j.algal.2013.11.002. Quinn, J., Winter, L., Bradley, T., 2011. Microalgae bulk growth model with application to industrial scale systems. Biores. Technol. 102 (8), 5083e5092. http:// dx.doi.org/10.1016/j.biortech.2011.01.019. Rawat, I., Ranjith, R.K., Mutanda, T., Bux, F., 2011. Dual role of microalgae: phycoremediation of domestic wastewater and biomass production for sustainable biofuels production. Appl. Energy 88 (10), 3411e3424. http://dx.doi.org/ 10.1016/j.apenergy.2010.11.025. Razon, L.F., Tan, R.R., 2011. Net energy analysis of the production of biodiesel and biogas from the microalgae: Haematococcus pluvialis and Nannochloropsis. Appl. Energy 88 (10), 3507e3514. Rickman, M., Pellegrino, J., Hock, J., et al., 2013. Life-cycle and techno-economic analysis of utility-connected algae systems. Algal Res. 2 (1), 59e65. http:// dx.doi.org/10.1016/j.algal.2012.11.003. Rogers, J.N., Rosenberg, J.N., Guzman, B.J., et al., 2013. A critical analysis of paddlewheel-driven raceway ponds for algal biofuel production at commercial scales. Algal Res. http://dx.doi.org/10.1016/j.algal.2013.11.007.

Sander, K., Murthy, G.S., 2010. Life cycle analysis of algae biodiesel. Int. J. Life Cycle Ass. 15, 704e714. http://dx.doi.org/10.1007/s11367-010-0194-1. Scott, S.A., Davey, M.P., Dennis, J.S., et al., 2010. Biodiesel from algae: challenges and prospects. Curr. Opin. Biotechnol. 21 (3), 277e286. http://dx.doi.org/10.1016/ j.copbio.2010.03.005. Sforza, E., Bertucco, A., Morosinotto, T., Giacometti, G.M., 2011. Photobioreactors for microalgal growth and oil production with Nannochloropsis salina: from labscale experiments to large-scale design. n. December Chem. Eng. Res. Des., 1e8. http://dx.doi.org/10.1016/j.cherd.2011.12.002. Institution of Chemical Engineers. Sheehan, J., Dunahay, T., Benemann, J., Roessler, P., 1998. A Look Back at the U.S. Department of Energy’s Aquatic Species ProgramdBiodiesel from Algae. National Renewable Energy Laboratory (NREL). Available at: http://www1.eere. energy.gov/biomass/pdfs/biodiesel_from_algae.pdf. Singh, A., Olsen, S.I., 2011. A critical review of biochemical conversion, sustainability and life cycle assessment of algal biofuels. Appl. Energy. http://dx.doi.org/ 10.1016/j.apenergy.2010.12.012. Stephenson, A.L., Kazamia, E., Dennis, J.S., et al., 2010. Life-cycle assessment of potential algal biodiesel production in the United Kingdom: a comparison of raceways and air-lift tubular bioreactors. Energy Fuels 24 (7), 4062e4077. http://dx.doi.org/10.1021/ef1003123. U.S. DOE, 2010. National Algal Biofuels Technology Roadmap. U.S. Department of Energy, Office of Energy Efficiency and Renewable Energy, Biomass Program. Available at: http://biomass.energy.gov. Udom, I., Zaribaf, B.H., Halfhide, T., et al., 2013. Harvesting microalgae grown on wastewater. Bioresour. Technol. 139, 101e106. http://dx.doi.org/10.1016/ j.biortech.2013.04.002. Uduman, N., Qi, Y., Danquah, M.K., Forde, G.M., Hoadley, A., 2010. Dewatering of microalgal cultures: a major bottleneck to algae-based fuels. Renew. Sustain. Energy 2, 012701. http://dx.doi.org/10.1063/1.3294480. Um, B.H., Kim, Y.S., 2009. Review: a chance for Korea to advance algal-biodiesel technology. J. Ind. Eng. Chem. 15 (1), 1e7. http://dx.doi.org/10.1016/ j.jiec.2008.08.002. Weschler, M.K., Barr, W.J., Harper, W.F., et al., 2014. Process energy comparison for the production and harvesting of algal biomass as a biofuel feedstock. Bioresour. Technol. 153, 108e115. http://dx.doi.org/10.1016/j.biortech.2013.11.008. Yang, J., Xu, M., Zhang, X., et al., 2011. Life cycle analysis on biodiesel production from microalgae: water footprint and nutrients balance. Bioresour. Technol. http://dx.doi.org/10.1016/j.biortech.2010.07.017. Yoo, C., Jun, S.Y., Lee, J.Y., Ahn, C.Y., Oh, H.M., 2010. Selection of microalgae for lipid production under high levels carbon dioxide. Bioresour. Technol. 101 (1), S71eS74. http://dx.doi.org/10.1016/j.biortech.2009.03.030. €ni, H., Gauch, M., Hischier, R., Lehmann, M., Wa €ger, P., 2009. Life Cycle Zah, R., Bo Assessment of Energy Products: Environmental Impact Assessment of Biofuels. Executive Summary. Empa, Technology and Society Lab, Lerchenfeldstrasse 5, CH-9014 St. Gallen, Switzerland. Zhang, Y., Colosi, L.M., 2013. Practical ambiguities during calculation of energy ratios and their impacts on life cycle assessment calculations. Energy Policy 57, 630e633. http://dx.doi.org/10.1016/j.enpol.2013.02.039.

Please cite this article in press as: Medeiros, D.L., et al., Energy production from microalgae biomass: carbon footprint and energy balance, Journal of Cleaner Production (2014), http://dx.doi.org/10.1016/j.jclepro.2014.07.038