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Bioresource Technology 245 (2017) 162–170

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Autotrophic and heterotrophic microalgae and cyanobacteria cultivation for MARK

food and feed: life cycle assessment

Sergiy Smetanaa, , Michael Sandmannb, Sascha Rohnb, Daniel Pleissnerc, Volker Heinza
German Institute of Food Technologies – DIL e.V., Prof.-von-Klitzing-Str. 7, 49610 Quakenbrueck, Germany
Institute for Food and Environmental Research (ILU) e.V., Arthur-Scheunert-Allee 40/41, Nuthetal, Germany
Sustainable Chemistry (Resource Efficiency), Institute of Sustainable and Environmental Chemistry, Leuphana University of Lüneburg, Scharnhorststr. 1, C13.203, 21335
Lüneburg, Germany


Keywords: The lack of protein sources in Europe could be reduced with onsite production of microalgae with autotrophic
Open raceway ponds and heterotrophic systems, owing the confirmation of economic and environmental benefits. This study aimed at
Tubular photobioreactor the life cycle assessment (LCA) of microalgae and cyanobacteria cultivation (Chlorella vulgaris and Arthrospira
Fermenter platensis) in autotrophic and heterotrophic conditions on a pilot industrial scale (in model conditions of Berlin,
Germany) with further biomass processing for food and feed products. The comparison of analysis results with
Cyanobacteria LCA
traditional benchmarks (protein concentrates) indicated higher environmental impact of microalgae protein
powders. However high-moisture extrusion of heterotrophic cultivated C. vulgaris resulted in more en-
vironmentally sustainable product than pork and beef. Further optimization of production with Chlorella pyr-
enoidosa on hydrolyzed food waste could reduce environmental impact in 4.5 times and create one of the most
sustainable sources of proteins.

1. Introduction premium quality (Balogh et al., 2016; Johnson and Wardle, 2014).
Market is getting enriched with meat substitutes of vegetable origin
The world is facing a problem of supplying high quality food to a using their healthier and more sustainable character as a leveraging
constantly increasing population. With predicted 9 billion people in market tool. However, the progression of vegetable analogs on Eur-
2050, food production should increase by 70% (FAO, 2009) but this opean market depends also on confirmed prime nutrition comparing to
triggers higher risks for human health through environmental pollution. traditional meat-based products, which in many cases is a limiting
The facets of the future food supply problem are already observed in a factor for vegan or vegetarian diets (Clarys et al., 2014).
form of food and feed protein sources lack and malnutrition in many Therefore, this paradox of choice between highly nutritional and
regions of the world (De Onis et al., 1993). In Europe, the biggest highly impacting animal-based products and less nutritional and more
“protein” problem relates to the import of the most (70–80%) of feed sustainable vegetable-based foods is triggering a development of a wide
protein concentrates (FAO, 2017). Such feed requirements are re- range of meat substitutes based on mycoproteins, insect biomass, fer-
flecting the increased demand for meat in Europe and beyond. The lack mentation proteins and microalgae (Kumar et al., 2017; Smetana et al.,
of protein sources in Europe is triggering the search for more sustain- 2016; Smetana et al., 2015). The substitution of meat with plant or
able solutions than current “cheap” feed from overseas. One of the microorganism based substitutes produced in biorefineries under con-
foreseen solutions is the limitation of meat consumption via govern- sideration of a closed resource cycle is considered as a possible resol-
mental regulations (Kromhout et al., 2016). But many authors claim ving solution for more sustainable food system (Aiking, 2011; De Boer
that such approach has limitation and drawbacks (such as traditional et al., 2006). At the same time, while for many food substitutes there
behavior of meat consumption and dietary preferences associated with are studies reflecting on their sustainability state (Smetana et al., 2016;
the level of income) which would reduce its effectivity (Block et al., Smetana et al., 2015), an adequate analysis for microalgae is missing.
2004; Drewnowski and Popkin, 1997). Microalgae and cyanobacteria (often misleadingly named micro-
Another approach is relying more on market mechanisms of con- algae as well) are a promising source of proteins for food and feed
sumers seeking for a greater variety of products of additional value or purposes (Draaisma et al., 2013; Milledge, 2011; Wijffels and Barbosa,

Corresponding author.
E-mail address: (S. Smetana).
Received 28 June 2017; Received in revised form 14 August 2017; Accepted 18 August 2017
Available online 20 August 2017
0960-8524/ © 2017 Elsevier Ltd. All rights reserved.
S. Smetana et al. Bioresource Technology 245 (2017) 162–170

Fig. 1. System boundaries and main scenarios of microalgae production (E0.6 – main input parameters affecting the production flow; E – energy in GWh, including electricity for heating,
processing and solar energy;∼E – energy in MWh; F – total fertilizers in ton; W – water including rainwater in kton; WR – water recycled in kton; GC – gas CO2 in ton; GG – glucose in ton;
EW11t – evaporated water in ton; 90% – allocation factor for the fractionated products; P 1.7 t – protein meal concentrate in ton; O 0.1 t – extracted microalgae oil in ton; FU – functional
unit; S – A. platensis; C – C. vulgaris; ORP – open raceway pond; TBR – tubular photobioreactor; HTF – heterotrophic fermenter.

2010; le Williams and Laurens, 2010; Wijffels et al., 2010). Moreover, of the same production level (a step missing in many LCA of microalgae
microalgae (as a source of proteins) are known to represent beneficial production in literature). Moreover, FU considered variations in the
nutritional qualities (Spolaore et al., 2006), but economic and en- properties of harvested microalgae biomass and further produced food
vironmental benefits of their production are questionable. That is why and feed. The inclusion of such variations of microalgae production and
life cycle assessment (LCA) of microalgae-based products and their processing allowed to cover the scope “from cradle to processing gate”
comparison with more traditional protein foods is the main purpose of with system expansion to the potential by-product generation and/or
this study. Additionally, the results of the LCA should provide an insight waste treatment at cultivation and processing stages.
on the use of microalgae for feed purposes. The presented LCA was divided into four main parts: (1) modelling
This article focused on LCA of microalgae and cyanobacteria (fur- and analysis of microalgae production under autotrophic and hetero-
ther microalgae) application for food and feed purposes, based on trophic conditions at the same production scale; (2) processing of the
models for pilot industrial scale of cultivation and processing. It high- microalgae biomass into food and feed suitable products; (3) compar-
lights a few main issues associated with comparability of technologies ison of microalgae-based food and feed products with more traditional
and their upscaling issues in upstream and downstream production benchmarks; and (4) sensitivity analysis and identification of more
processes. Multiple microalgae species, variations in their cultivation sustainable scenarios of microalgae production. The assessment fol-
and processing make the sustainability assessment challenging and not lowed the standard LCA approach (ISO, 2006a,b) and used professional
always reliable due to the variations in scales and approaches. The goal SimaPro8 software and adapted ecoinvent 3.1 datasets for background
of the research is the systematic LCA of generic microalgae production data (electricity and water supply, heat generation, etc.). At the same
(with two model species: Chlorella vulgaris and Arthrospira platensis) for time, the study relied on the simultaneous use of two midpoint impact
food and feed products. Additional points of the article would touch the assessment methods (ReCiPe V1.08 and IMPACT 2002+) (Goedkoop
environmental improvement potential of alternative strains cultivation et al., 2013; Jolliet et al., 2003) to get the possible variation ranges of
(Chlorella pyrenoidosa), use of different feeds and resource inputs and main midpoint characterization factors and exclude the limitations of
further processing (high-moisture extruded products, extracted oils and both methods. For the integrated results interpretation, the study based
protein meals). The outcomes of the article indicating the most pro- on the similar endpoint impact assessment methodologies.
mising scenarios of more sustainable microalgae production for food
and feed purposes in environmental perspective will be interesting for
food and feed producers, policy makers and scientists. 2.1.2. Type of LCA
The study relied on attributional LCA approach with via inclusion of
waste treatment allocated to the main product(s) to assess the estab-
2. Methods and materials lished and innovative options of microalgae cultivation. The potential
impact of food system transformation due to the microalgae production
2.1. Life cycle assessment (consequential approach) was not considered. However, the study fol-
lowed a “prospective attributional approach” (Hospido et al., 2010)
2.1.1. Goal and scope of the study aiming to indicate the advantages (or disadvantages) of microalgae-
The goal of the study was to perform a LCA of different ways of based food and feed in comparison with traditional alternatives pro-
microalgae production and processing at industrial pilot scale and duced via current state technologies and compared to different steady
compare the results with traditional benchmark products (food and states (without possible future implications included). Attributional
feed). The results were expected to provide and answer on the claims of approach in LCA required allocation of environmental impact between
better environmental sustainability of microalgae use for food and feed microalgae biomass products (oil and proteins), which was performed
purposes. Such approach required the setting of a proper functional unit according to economic values. System expansion was applied to the
(FU), system boundaries and assurance of data quality. FUs considered scenarios of waste and side-streams application as microalgae nutrition
in the study included the modelling of microalgae production facilities sources.

S. Smetana et al. Bioresource Technology 245 (2017) 162–170

Table 1
Life cycle inventory of microalgae production and processing.

Scenarios Cultivation, per FU1 Initial processing, per Whole dry microalgae Fractionation processing, per
FU1 processing, per FU2 FU2

CORP Inputs
NG: 124.7 kWh; Electricity: 3.56 kWh; Water: 0.58 m3; Gas (CO2): Electricity: 0.26 kWh; FB: 7.1 kg; DPP: 1 kg;
0.37 kg; Land: 0.1 m2; F: 0.04 kg N, 0.02 kg P Electrodes (Fe, Al): Electricity: 14.25 kWh Electricity: 0.7 kWh
0.002 kg
Wastewater: 0.09 m3; EW: 0.15 m3; CO2 emissions: 0.07 kg FB: 1 kg; DPP: 1 kg; PMP: 0.85 kg;
RW: 0.55 m3; EW: 6.0 kg Oil: 0.15 kg
Wastewater: 0.06 m3

SORP Inputs
NG: 95.9 kWh; Electricity: 2.74 kWh; Water: 0.6 m3; Gas (CO2): 0.37 kg; Electricity: 0.34 kWh; FB: 7.2 kg; DPP: 1 kg;
Land: 0.08 m2; F: 0.04 kg N, 0.02 kg P Electrodes (Fe, Al): Electricity: 14.25 kWh Electricity: 0.7 kWh
0.002 kg
Wastewater: 0.13 m3; EW: 0.12 m3; CO2 emissions: 0.07 kg FB: 1 kg; DPP: 1 kg; PMP: 0.95 kg;
RW: 0.73 m3; EW: 6.1 kg Oil: 0.05 kg
Wastewater: 0.08 m3

CTBR Inputs
NG: 0.19 kWh; Electricity: 9.1 kWh; Water: 0.34 m3; Gas (CO2): 0.6 kg; Electricity: 0.02 kWh; FB: 7.0 kg; DPP: 1 kg;
HP: 0.06 m3; CA: 0.06 m3; Land: 0.06 m2; F: 0.02 kg N, 0.01 kg P Electrodes (Fe, Al): Electricity: 13.5 kWh Electricity: 0.7 kWh
0.002 kg
Wastewater: 0.42 m3; EW: 1.3 kg; CO2 emissions: 0.29 kg FB: 1 kg; DPP: 1 kg; PMP: 0.85 kg;
RW: 0.04 m3; EW: 6.0 kg Oil: 0.15 kg
Wastewater: 3.5 kg

STBR Inputs
NG: 0.15 kWh; Electricity: 7.6 kWh; Water: 0.3 m3; Electricity: 0.03 kWh; FB: 6.6 kg; DPP: 1 kg;
Gas (CO2): 0.61 kg; HP: 0.05 m3; CA: 0.05 m3; Land: 0.05 m2; F: Electrodes (Fe, Al): Electricity: 13.5 kWh Electricity: 0.7 kWh
0.02 kg N, 0.01 kg P 0.002 kg

Wastewater: 0.36 m3; FB: 1 kg; DPP: 1 kg; PMP: 0.95 kg;
EW: 0.8 kg; RW: 0.07 m3; EW: 5.5 kg Oil: 0.05 kg
CO2 emissions: 0.3 kg Wastewater: 6.3 kg

CHTF Inputs
NG: 0.002 kWh; Electricity: 0.17 kWh; Water: 0.01 m3; Gas (O2): Electricity: 0.007 kWh; FB: 7.0 kg; DPP: 1 kg;
0.004 kg; Glucose: 0.34 kg; HP: 2.4 m3; Steam: 0.5 kg; Land: 0.001 m2; Electrodes (Fe, Al): Electricity: 14.25 kWh Electricity: 0.7 kWh
F: 0.002 kg N, 0.001 kg P 0.002 kg

Wastewater: 6.1 kg; EW: 0.5 kg; CO2 emissions: 0.13 kg FB: 1 kg; DPP: 1 kg; PMP: 0.85 kg;
Wastewater: 0.01 kg EW: 5.9 kg Oil: 0.15 kg

Note: C – C. vulgaris; S – A. platensis; ORP – open raceway pond; TBR – tubular photobioreactor; HTF – heterotrophic fermenter; N – nitrogen; P – phosphorous; F – fertilizers; NG – natural
gas; FB – fresh biomass; RW – recycled water; DPP – dry protein powder; EW - evaporated water; HP - hydrogen peroxide 3% solution; CA – Citric acid 0.5%; PMP – protein meal powder.

2.1.3. Functional unit et al., 2010). Considering the variety of blue-green algae (2500–3000
The study aimed on the “fair” comparison of the microalgae culti- species), the possible variations for the microalgae production exceeds
vation systems, food and feed products generated based on the micro- thousand options (Metting, 1996). However, less than ten species are
algae biomass. In order to achieve this a few FU were used (Fig. 1). The allowed for the food consumption in European Union according to the
first FU (FU1) indicated the comparison of the microalgae cultivation Novel Food Regulation (Regulation EC, 1997). Moreover, the whole
systems at the stage of previous processing of biomass (flocculation and variety of cultivation systems could be presented in three main ag-
centrifugation). It was considered as 1 kg of fresh microalgae biomass gregated options: (1) autotrophic open ponds; (2) autotrophic closed
sludge (85–90% of moisture content). The second FU (FU2) included bio-reactors; and (3) heterotrophic closed fermenters. Therefore, these
the consideration of the whole dried microalgae biomass use in the three cultivation options were compared in this study: open raceway
form of protein powder (concentrate). The function of the protein pond (ORP), tubular photobioreactor (TBR), and heterotrophic fer-
powder use was considered as supplying food and feed products with menter (HTF). Among the variety of microalgae and cyanobacteria, two
specific amount of proteins. Then the third FU (FU3) was 1 kg of bulk species were selected (C. vulgaris and A. platensis) as the most widely
proteins supplied in a form of powder concentrate meal remaining from presented in the literature indicating their potential use for food pur-
defatting of whole dried protein powder. Such consideration allowed poses (Milledge, 2011; Vigani et al., 2015). And one more strain
the differentiation of microalgae production according to the species (Chlorella pyrenoidosa) was used for sensitivity analysis. The study in-
and production conditions. The fourth FU (FU4) was used for the esti- cluded three main system boundaries associated with microalgae bio-
mation of environmental impacts of microalgae oils used for food mass cultivation and processing into food and feed products (Fig. 1).
purposes (1 kg of oil). The first system responded to the first FU and aimed at the production
of fresh biomass (“from cradle to gate” of microalgae cultivation). The
2.1.4. System boundaries other two system boundaries additionally included further processing
Microalgae cultivation and processing could be performed in a great of the biomass into protein powders, protein concentrates and oils.
variety of systems (Brentner et al., 2011; Bux and Chisti, 2016; Gao

S. Smetana et al. Bioresource Technology 245 (2017) 162–170

Fig. 2. Comparison of microalgae cultivation technologies with end-point impact categories: FU1 – 1 kg of fresh microalgae biomass; mPt – millipoints (ecopoints, 1 kPt is equal to the
annual impact of one European citizen); CORP – open raceway pond cultivation of C. vulgaris; SORP – open raceway pond cultivation of A. platensis; CTBR – tubular photobioreactor
cultivation of C. vulgaris; STBR – tubular photobioreactor cultivation of A. platensis; CHTF – heterotrophic fermenter cultivation of C. vulgaris.

2.2. Scenarios during processing trials in German Institute of Food Technologies (DIL
e.V.; Quakenbrueck, Germany) and in Institute for Food and Environ-
The study included five initial scenarios for the cultivation of mi- mental Research (ILU e.V.; Nuthetal, Germany) and partially from lit-
croalgae (two species and three cultivation methods, with exclusion of erature sources (Brentner et al., 2011; Bux and Chisti, 2016; Handler
heterotrophic cultivation of A. platensis due to the low efficiency of et al., 2014, 2012; Vandamme et al., 2013). Background data on pro-
production). In order to reflect the variety of selected processing duction of resources (electricity, heat, fertilizers), as well as the agri-
methods for food and feed, three main resulting products were included cultural stage of alternative feeds were based on data from ecoinvent
(whole dried microalgae powder, high-moisture extruded product and 3.1 (Zurich, Switzerland) adapted to the study conditions (Table 1).
microalgae extracts). Together with additional scenarios designed to
reflect the potential of alternative feeds use for microalgae cultivation,
the study additionally considered a few secondary scenarios, designed 2.4. Assumptions
like a part of sensitivity analysis. Such approach allowed the estimation
of influence of system boundaries, FUs and allocation rules (Fig. 1). The study relied on a number of conclusions made based on current
Sensitivity analysis, aimed for the optimization of microalgae produc- scientific literature and personal communications with experts in the
tion, included additional scenarios: consideration of microalgae Chlor- field. It was assumed that the microalgae production in all three sce-
ella pyrenoidosa, selection of energy sources and change of processing, narios took place in Berlin, Germany. Such an assumption resulted in
feeding substances, and climate conditions. the need to include heating (and cooling) of cultivation media, which
resulted in high heat requirements for scenarios based on open raceway
ponds and tubular photobioreactors. All the scenarios relied on the use
2.3. Data sources of energy mix typical for Germany (ecoinvent 3 database) for the
consideration of electricity use. The main sources of carbon consisted of
The study relied on several sources used for the cultivation model atmosphere air with addition of concentrated CO2 for ORP and TBR
construction. From one side the relevant literature sources on the cul- scenarios and glucose (sugar beet production) for HTF scenario.
tivation of Chlorella and Spirulina in specific conditions (Bux and Chisti, Initial cultivation of seed microalgae media was excluded from
2016; De Visser et al., 2014; Li et al., 2007; Perez-Garcia and Bashan, model scenarios due to the minor role and impact. Processing of mi-
2015; Schipperus et al., 2014; White et al., 2015) were considered. croalgae biomass included a few stages. First microalgae media un-
From the other side LCA models were supported with data on lab scale derwent electrical flocculation (was selected to provide a high-quality
cultivation of Chlorella from Institute of Sustainable and Environmental biomass suitable for food purposes) and centrifugation, which allowed
Chemistry (Leuphana University of Lüneburg, Lüneburg, Germany) and to eliminate extra moisture and recycle it (ORP and TBR scenarios).
pilot scale cultivation and processing of Spirulina from Institute for Food Further processing included lyophilisation (freeze-drying) and fractio-
and Environmental Research (ILU e.V.; Nuthetal, Germany). Fore- nation (separation of oil from dry powder biomass). Microalgae pro-
ground data of microalgae biomass processing was partially collected cessing models also enclosed assumption for the downtime and losses in

S. Smetana et al. Bioresource Technology 245 (2017) 162–170

microalgae cultivation due to technical failures and cleaning proce- et al., 2011; Handler et al., 2014; Vandamme et al., 2013), these im-
dures. Cleaning procedures in TBR scenarios consisted of treatment via pacts were of a relatively low importance in this study.
3% hydrogen peroxide and 0.5% citric acid, HTF scenarios excluded The comparison of environmental impacts of whole microalgae
treatment with citric acid but and additionally relied on sterilization protein powder modelled in current study with more traditional protein
with steam. Fractionation (separation of oil and protein biomass) con- concentrates used for food and feed (Table 2) indicated that ORP and
sisted of bed milling and supercritical CO2 extraction (Brentner et al., PBR scenarios were more environmentally impacting than most tradi-
2011). tional sources. However, they were in the same range of impact in ca-
tegories of freshwater depletion and land use. CHTF scenario despite
3. Results and discussion being the most environmentally promising way to produce microalgae
in conditions of Germany (Berlin), still had relatively high impacts in
3.1. Cultivation of biomass categories of land use, energy use and global warming potential (con-
nected to glucose use as a source of carbon). Such results indicated that
Most of the scenarios of microalgae biomass cultivation relied on use of microalgae as food protein powder concentrate was not more
the similar scale of production. According to the studies (De Visser environmentally friendly than vegetable sources and in the same range
et al., 2014; Li et al., 2007; Schipperus et al., 2014) it was estimated of impact as animal derived sources of proteins. Therefore, the en-
that the functioning of ORP with a volume of 300 m3, PBR – of 25 m3 vironmental sustainability of microalgae protein powders should not be
and HTF – of 2.5 m3 would provide the similar amount of biomass claimed without justification.
(1.4–1.8 ton dry matter year−1). Owning the low efficiency of A. pla-
tensis production in heterotrophic conditions, relevant scenario was 3.3. Extracted protein and oil-based products
excluded from LCA. Among the other scenarios (Fig. 2) the highest
environmental impact was indicated for the microalgae production via Microalgae are commonly used for the production of oil for biofuel
ORP for both species (7.7–9.7 mPt). TBR scenarios had impact in the purposes and protein biomass for food and feed (Shi et al., 2017). At the
range of 4–4.7 mPt with more beneficial results for A. platensis. The same time, microalgae are considered as a source of valuable bioactive
least environmentally impacting scenario was heterotrophic cultivation compounds (e.g. pigments, vitamins, enzymes) and multiple production
of C. vulgaris with overall environmental impact of 0.4 mPt. and extraction methods are developed (Chew et al., 2017; Matos et al.,
The highest impact was indicated for categories of non-renewable 2017). That is why current study identified potential environmental
energy consumption, global warming and respiratory inorganics emis- benefits of extracted oil and bulk proteins from microalgae (according
sions. The impacts were associated with cultivation of microalgae (for to the identified microalgae production scenarios). They were perceived
scenarios CORP and SORP) and with cleaning procedures (for scenarios as raw components further applicable for various purposes (functional
CTBR and STBR). Scenario CHTF was characterized with impacts gen- foods, nutraceuticals, and biofuel).
erated using glucose and electricity for cultivation. Therefore, the The comparison results (Fig. 4) identified that the differentiation of
limitation of microalgae production as a viable source of protein bio- environmental impacts became more evident for oils (scenarios with C.
mass was connected with the low concentration of microalgae in high vulgaris had higher environmental impact) while for protein meals
volumes of water, which should be kept in a constant dynamic state, concentrates the difference between species was negligible. It was
cooled or warmed due to the changing environmental conditions. connected with environmental impact allocation due to a higher price
of microalgae oil than protein meal (used as feed in most cases).
3.2. Protein powder concentrates However, further extraction of specific high-value protein components
could change the allocation rules if economic conditions were con-
The cultivation of microalgae included flocculation and cen- sidered (possibility for further studies).
trifugation in order to get concentrated fresh biomass “soup” or fresh
biomass reviewed in previous chapter. The simplest further processing 3.4. Moisturized protein products
and application for food purposes included drying of the biomass to the
state of powder. In order to preserve the valuable components of mi- Another potential use of whole dried microalgae protein powder
croalgae cells (e.g. proteins) the study did not rely on common thermal includes its use as a component of more complex food products. For
methods (spray, oven or drum drying). Instead, gentler and nutrient example, high-moisture extrusion incorporates mixing of the compo-
preserving lyophilisation (freeze-drying) was considered for protein nents (powder and water), dynamic cooking under increased pressure
powders production from whole microalgae in current study. The sen- and temperature conditions (up to 170 °C) with further cooling in a
sitivity analysis included verification of the method change for relevant cooling dye, which allows forming a fiber meat-like texture of a pro-
scenarios. duct. High-moisture extrudates (HME) are also characterized with the
The distribution of results (Fig. 3) for FU of 1 kg of protein powder main nutritional properties similar to those in meat. Dried whole A.
concentrate (4% moisture content) were similar to the results of fresh platensis was tested for the ability to be used as a raw component for the
biomass comparison (Fig. 2). The protein powder concentrates pro- extrusion in DIL e.V. (Quakenbrueck, Germany), where it was possible
duced via OPR scenarios had higher impact comparing to the scenarios to reach the rate of inclusion from 30% (in combination with soya
based on TBR or HTF (Chlorella only). Such results were logical due to protein concentrate) to 75% (in combination with soya protein con-
similar technological process of fresh biomass processing into dry centrate and carrageenan) (DIL e.V., personal communication). The
protein powder. development of high-moisture extruded meat substitutes based on au-
High energy consumption rates in CORP and SORP scenarios were totrophic microalgae biomass resulted in green-colored products which
related to the need of maintaining of stable temperature conditions had higher environmental impacts than soy-based meat substitute, but
throughout a year. It included the need to warm up ORP and TBR in were comparable in environmental impact to meat (Fig. 5). Moreover,
winter months and cool them down in summer and to mix the fluid in meat substitutes based on soybean meal and heterotrophically pro-
the systems. Such results indicated environmental “hotspots”, asso- duced Chlorella protein powder had lower environmental impact than
ciated with the need to select optimal climate conditions for cultivation pork and chicken meat. These results were very promising as they in-
of systems, which requite high volumes of water for the production. At dicated that despite overall high inefficiency of the most common mi-
the same time, the processing of the biomass was responsible for 5–10% croalgae cultivation methods, there was a possibility for further im-
of environmental impact only. Even though, many literature sources provements. It was not possible to recommend the use of microalgae
indicate high energy requirements for microalgae processing (Brentner biomass for feed as more environmentally friendly alternative. At the

S. Smetana et al. Bioresource Technology 245 (2017) 162–170

Fig. 3. Environmental impact of whole microalgae protein powder FU2 – 1 kg of dried whole microalgae biomass; mPt – millipoint (ecopoint, 1 kPt is equal to the annual impact of one
European citizen); CORP – open raceway pond cultivation of C. vulgaris; SORP – open raceway pond cultivation of A. platensis; CTBR – tubular photobioreactor cultivation of C. vulgaris;
STBR – tubular photobioreactor cultivation of A. platensis; CHTF – heterotrophic fermenter cultivation of C. vulgaris.

Table 2
Environmental impact comparison of main protein sources used for food and feed (per 1 kg of protein meal or powder).

DM% Protein,% of GWP, kg CO2 eq. OD, mg AC, g SO2 eq. EU, g N eq. ED, MJ FD, m3 LU, m2a
DM CFC11 eq.

Soybean meal 87.51 49.11 0.34–0.72 1

0.2–0.271 −1.2 to 3.11 −81 to 21 (g NO3 5.376 0.046 3.266
Rapeseed cake 891 34.81 0.37–0.576 0.004–0.056 6.8–7.56 8.9–9.16 3.3–3.86 0.001–0.036 1.5–1.66
Pea protein meal n/a n/a 0.446 0.0576 21.86 7.946 5.256 0.036 2.856
4–108 (pulses)
Whey concentrate 86–893 603,7 7.487 3.337 56.67 37.32 58.12 1.452 0.26–8.276
0.8–7.4612.1228–438 (kg 0.01–0.069 0.05–1.56 1.146 83.37 9.587
protein) 3.59–1019 10.7–39.46 0.003–0.0666
Egg protein 853 803 23.43 1.013 40003 1393 1833 2.653 40.13
Fishmeal 904 60–725 0.8844 1.034 18.04 −164 15.84 0.3474 n/a
Chlorella HTF3 96 55 14.7 0.9 260.5 40.6 217.1 0.3 4.8
Chlorella ORP3 96 55 245.1 19.8 1407.5 42.2 4181.3 3.3 1.9
Chlorella TBR3 96 55 96.1 8.9 1143.0 105.3 1516.2 3.9 5.4
Spirulina ORP3 96 55 196.3 15.9 1165.0 49.2 3338.3 3.2 1.7
Spirulina TBR3 96 55 78.1 7.2 915.9 85.3 1225.6 3.3 4.3

Sources: 1 – (Dalgaard et al., 2008); 2 – (Kim et al., 2013); 3 – own calculations, 4 – Danish LCA Food Database; 5 – (Hall, 2011); 6 – ecoinvent 3 and Agrifootprint databases; 7 – (Smetana
et al., 2016); 8 – (Nijdam et al., 2012). Note: HTF – heterotrophic fermenter; ORP – open raceway pond; TBR – tubular bioreactor; DM – dry mass, GWP – global warming potential; OD –
ozone depletion; AC – acidification; EU – eutrophication; ED – energy demand; FD – freshwater depletion; LU – land use.

same time application of heterotrophic microalgae for high-moisture optimized scenarios. They included heterotrophic production of C.
extrusion of meat substitutes could result in more environmentally vulgaris fed on alternative to glucose source of carbon (26% of en-
perspective food protein products. vironmental impact), change of biomass drying method, alternative mix
and source of electricity (51% of impact), open raceway pond pro-
duction of A. platensis in more favorable climate conditions (more than
3.5. Sensitivity analysis 80% of impact associated with heating); heterotrophic production of
alternative microalgae strain (C. pyrenoidosa) fed on alternative carbon
Based on the results of LCA for the scenarios of the current study, source – food waste composed of rice, noodles, meat and vegetable
the sensitivity analysis concentrated on reviewing potentially more

S. Smetana et al. Bioresource Technology 245 (2017) 162–170

Fig. 4. End point categories environmental impact of microalgae products: FU3 – 1 kg of dried defatted protein meal; FU4 – 1 kg of microalgae oil; mPt – millipoint (ecopoint, 1 kPt is
equal to the annual impact of one European citizen); CORP – open raceway pond cultivation of C. vulgaris; SORP – open raceway pond cultivation of A. platensis; CTBR – tubular
photobioreactor cultivation of C. vulgaris; STBR – tubular photobioreactor cultivation of A. platensis; CHTF – heterotrophic fermenter cultivation of C. vulgaris.

mixture collected from canteens (Pleissner et al., 2013). The results increased water consumption due to intensified evaporation in the arid
indicated that there was a potential for the improvement of microalgae conditions. Despite the reduction of environmental impact open ra-
production with the use of alternative sources of carbon (glycerol) and/ ceway ponds scenarios remained high in environmental impact. It can
or strain of microalgae (food waste and C. pyrenoidosa) (Fig. 6). be summarized that environmental conditions affected the cultivation
Cultivation of A. platensis in more favorable climate conditions of autotrophic microalgae, but did not change their relative to other
(Tenerife, Spain) resulted in reduction of environmental impact (by scenarios performance and remain similar to those in other conditions
25%) due to the reduced need in OPR heating, but at the same time of Europe.

Fig. 5. End-point categories environmental impact of fresh meat and high-moisture extruded intermediates: results for 1 kg of fresh product; mPt – millipoint (ecopoint, 1 kPt is equal to
the annual impact of one European citizen); CPBR – tubular photobioreactor cultivation of C. vulgaris; SPBR – tubular photobioreactor cultivation of A. platensis; CHTF – heterotrophic
fermenter cultivation of C. vulgaris.

S. Smetana et al. Bioresource Technology 245 (2017) 162–170

Fig. 6. End-point categories environmental impact of whole microalgae protein powder FU2 – 1 kg of dried whole microalgae biomass; mPt – millipoint (ecopoint, 1 kPt is equal to the
annual impact of one European citizen); CHTF – heterotrophic fermenter cultivation of C. vulgaris; CHTF_AE – CHTF scenario with use of photovoltaic energy as a source of electricity;
CHTF_G – CHTF scenario with use of glycerol like a source of carbon for cultivation; CPHTF_W – heterotrophic fermenter cultivation of C. pyrenoidosa with use of food waste as a source of
carbon for cultivation; CHTF_AP – scenario with alternative drying of biomass (oven); SORP – open raceway pond cultivation of A. platensis; SORP_T – open raceway pond cultivation of A.
platensis in alternative climate conditions (Tenerife, Spain).

The change of energy sources in heterotrophic production of mi- support was given by the German Ministry of Economics and Energy
croalgae has a potential of environmental impact reduction by 40%, (via AiF) and the FEI (Forschungskreis der Ernaehrungsindustrie e.V.,
while the change of carbon source could reduce the impact by 25–40%. Bonn), project AiF 129 EBG.
The most promising scenario in this case would be the combination of
microalgae production in heterotrophic conditions with the use of food References
waste as a source of carbon and photovoltaic energy generation for
cultivation. Such scenario would result in the production of protein Aiking, H., 2011. Future protein supply. Trends Food Sci. Technol. 22, 112–120. http://
concentrate powder, which would have an integrated environmental
Balogh, P., Békési, D., Gorton, M., Popp, J., Lengyel, P., 2016. Consumer willingness to
impact of 0.98 mPt for 1 kg (GWP: 2.25 kg CO2 eq., ED: 28.4 MJ, LU: pay for traditional food products. Food Policy 61, 176–184.
0.31 m2a) and would be one of the most beneficial protein sources 1016/j.foodpol.2016.03.005.
(Table 2). This final result of LCA modelling indicated the re- Block, J.P., Scribner, R.A., DeSalvo, K.B., 2004. Fast food, race/ethnicity, and income: a
geographic analysis. Am. J. Prev. Med. 27, 211–217.
commended path for further research and innovation activities, aiming Brentner, L.B., Eckelman, M.J., Zimmerman, J.B., 2011. Combinatorial life cycle assess-
to create a more sustainable system of alternative protein sources ment to inform process design of industrial production of algal biodiesel. Environ.
production. Sci. Technol. 45, 7060–7067.
Bux, F., Chisti, Y. (Eds.), 2016. Algae Biotechnology: Products and Processes. Springer.
Chew, K.W., Yap, J.Y., Show, P.L., Suan, N.H., Juan, J.C., Ling, T.C., Lee, D.-J., Chang, J.-
4. Conclusion S., 2017. Microalgae biorefinery: high value products perspectives. Bioresour.
Technol. 229, 53–62.
Clarys, P., Deliens, T., Huybrechts, I., Deriemaeker, P., Vanaelst, B., De Keyzer, W.,
Pilot industrial scale (1.4–1.8 ton dry matter year−1) of A. platensis Hebbelinck, M., Mullie, P., 2014. Comparison of nutritional quality of the vegan,
and C. vulgaris production with autotrophic (open raceway pond, tub- vegetarian, semi-vegetarian, pesco-vegetarian and omnivorous diet. Nutrients 6,
ular photobioreactor) and heterotrophic (fermenter) systems had
Dalgaard, R., Schmidt, J., Halberg, N., Christensen, P., Thrane, M., Pengue, W.A., 2008.
higher environmental impacts than production of most traditional food LCA of soybean meal. Int. J. Life Cycle Assess. 10, 240–254.
and feed protein sources. High impacts related to heat and energy use 1065/lca2007.06.342.
(autotrophic cultivation) and glucose for microalgae feed (hetero- De Boer, J., Helms, M., Aiking, H., 2006. Protein consumption and sustainability: diet
diversity in EU-15. Ecol. Econ. 59, 267–274.
trophic). Heterotrophic cultivated protein biomass applied for high- De Onis, M., Monteiro, C., Akré, J., Clugston, G., 1993. The worldwide magnitude of
moisture extrusion products was more beneficial than pork and beef. protein-energy malnutrition: an overview from the WHO Global Database on Child
Further optimization of production with C. pyrenoidosa on hydrolyzed Growth. Bull. World Health Org. 71, 703–712.
De Visser, C., Schipperus, R., Spruijt, J., Kootstra, M., 2014. AlgaEconomics. Output
food waste could provide more beneficial protein concentrate (2.25 kg WP2A7.03 Economic model for open pond cultivation v3.06.
CO2eq., 28.4 MJ, 0.31 m2a per 1 kg). Draaisma, R.B., Wijffels, R.H., (Ellen), P., Slegers, Brentner, L.B., Roy, A., Barbosa, M.J.,
2013. Food commodities from microalgae. Curr. Opin. Biotechnol. 24, 169–177.
Acknowledgements Drewnowski, A., Popkin, B.M., 1997. The nutrition transition: new trends in the global
diet. Nutr. Rev. 55, 31–43.
FAO, 2009. How to feed the world in 2050, Insights from an expert meeting at FAO.
This work was supported by Ministry for Science and Culture of FAO, 2017. Detailed trade matrix 1963-2013 [WWW Document]. URL http://www.fao.
Lower Saxony (Vorab programme) and Volkswagen Foundation in the org/faostat/en/#data/TM (accessed 6.10.17).
scope of the project “Sustainability transitions in food production: al- Gao, C., Zhai, Y., Ding, Y., Wu, Q., 2010. Application of sweet sorghum for biodiesel
production by heterotrophic microalga Chlorella protothecoides. Appl. Energy 87,
ternative protein sources in socio-technical perspective”. Additional

S. Smetana et al. Bioresource Technology 245 (2017) 162–170

756–761. review. Rev. Environ. Sci. Bio/Technol. 10, 31–41.

Goedkoop, M., Heijungs, R., De Schryver, A., Struijs, J., van Zelm, R., 2013. ReCiPe 2008. Nijdam, D., Rood, T., Westhoek, H., 2012. The price of protein: Review of land use and
A LCIA method which comprises harmonised category indicators at the midpoint and carbon footprints from life cycle assessments of animal food products and their
the endpoint level. Characterisation, A life cycle impact …. doi: http://www.lcia- substitutes. Food Policy 37, 760–770. 002.
Hall, G.M., 2011. Fish Processing: Sustainability and New Opportunities. John Perez-Garcia, O., Bashan, Y., 2015. Microalgal heterotrophic and mixotrophic culturing
Wiley & Sons. for bio-refining: from metabolic routes to techno-economics. In: Algal Biorefineries.
Handler, R.M., Canter, C.E., Kalnes, T.N., Lupton, F.S., Kholiqov, O., Shonnard, D.R., Springer, pp. 61–131.
Blowers, P., 2012. Evaluation of environmental impacts from microalgae cultivation Pleissner, D., Lam, W.C., Sun, Z., Lin, C.S.K., 2013. Food waste as nutrient source in
in open-air raceway ponds: Analysis of the prior literature and investigation of wide heterotrophic microalgae cultivation. Bioresour. Technol. 137, 139–146. http://dx.
variance in predicted impacts. Algal Res. 1, 83–92.
algal.2012.02.003. Regulation (EC), 1997. Regulation (EC) No 258/97 of the European Parliament and of the
Handler, R.M., Shonnard, D.R., Kalnes, T.N., Lupton, F.S., 2014. Life cycle assessment of Council of 27 January 1997 concerning novel foods and novel food ingredients. Off.
algal biofuels: Influence of feedstock cultivation systems and conversion platforms. J. Eur. Communities 40, 1–7.
Algal Res. 4, 105–115. Schipperus, R., De Visser, C., Spruijt, J., Kootstra, M., 2014. AlgaEconomics. Output
Hospido, A., Davis, J., Berlin, J., Sonesson, U., 2010. A review of methodological issues WP2A7.04 Economic model for tubular PBR cultivation v3.06.
affecting LCA of novel food products. Int. J. Life Cycle Assess. 15, 44–52. http://dx. Shi, X., Luo, Z., Chen, G.-H., Chen, F., Zhang, L.-H., Zhu, X.-M., Liu, X., 2017. Replacement of fishmeal by a mixture of soybean meal and chlorella meal in practical
ISO 14040, 2006. Environmental Management – Life Cycle Assessment – Principles and diets for Juvenile Crucian Carp, Carassius auratus. J. World Aquac. Soc. http://dx.
ISO 14044, 2006. Environmental Management – Life Cycle Assessment – Requirements Smetana, S., Mathys, A., Knoch, A., Heinz, V., 2015. Meat alternatives: life cycle assess-
and Guidelines. ment of most known meat substitutes. Int. J. Life Cycle Assess. 20, 1254–1267.
Johnson, F., Wardle, J., 2014. Variety, palatability, and obesity. Adv. Nutr. Int. Rev. J. 5,
851–859. Smetana, S., Palanisamy, M., Mathys, A., Heinz, V., 2016. Sustainability of insect use for
Jolliet, O., Margni, M., Charles, R., Humbert, S., Payet, J., Rebitzer, G., Robenbaum, R.K., feed and food: Life Cycle Assessment perspective. J. Clean. Prod. 137, 741–751.
2003. IMPACT 2002+: a new life cycle impact assessment methodology. Int. J. Life
Cycle Assess. 8, 324–330. Spolaore, P., Joannis-Cassan, C., Duran, E., Isambert, A., 2006. Commercial applications
Kim, D., Thoma, G., Nutter, D., Milani, F., Ulrich, R., Norris, G., 2013. Life cycle as- of microalgae. J. Biosci. Bioeng. 101, 87–96.
sessment of cheese and whey production in the USA. Int. J. Life Cycle Assess. 18, Vandamme, D., Foubert, I., Muylaert, K., 2013. Flocculation as a low-cost method for
1019–1035. harvesting microalgae for bulk biomass production. Trends Biotechnol. 31, 233–239.
Kromhout, D., Spaaij, C.J.K., de Goede, J., Weggemans, R.M., 2016. The 2015 Dutch food- Vigani, M., Parisi, C., Rodríguez-Cerezo, E., Barbosa, M.J., Sijtsma, L., Ploeg, M., Enzing,
based dietary guidelines. Eur. J. Clin. Nutr. 70, 869–878. C., 2015. Food and feed products from micro-algae: market opportunities and chal-
Kumar, P., Chatli, M.K., Mehta, N., Singh, P., Malav, O.P., Verma, A.K., 2017. Meat lenges for the EU. Trends Food Sci. Technol. 42, 81–92.
analogues: health promising sustainable meat substitutes. Crit. Rev. Food Sci. Nutr. tifs.2014.12.004.
57, 923–932. White, D., Silkina, A., Skill, S., Oatley-Radcliffe, D., Van Den Hende, S., Ernst, A., De
Li, X., Xu, H., Wu, Q., 2007. Large-scale biodiesel production from microalga Chlorella Viser, C., Van Dijk, W., Davey, M., Day, J., 2015. Best Practices for the Pilot-Scale
protothecoides through heterotrophic cultivation in bioreactors. Biotechnol. Bioeng. Cultivation of Microalgae, Public Output report of the EnAlgae project. Swansea.
98, 764–771. Wijffels, R.H., Barbosa, M.J., 2010. An outlook on microalgal biofuels. Science 329 (80),
Matos, J., Cardoso, C., Bandarra, N.M., Afonso, C., 2017. Microalgae as healthy in- 796–799.
gredients for functional food: a review. Food Funct. Wijffels, R.H., Barbosa, M.J., Eppink, M.H.M., 2010. Microalgae for the production of
C7FO00409E. bulk chemicals and biofuels. Biofuels Bioprod. Biorefining 4, 287–295.
Metting, F.B., 1996. Biodiversity and application of microalgae. J. Ind. Microbiol. 17, le Williams, P.J., Laurens, L.M.L., 2010. Microalgae as biodiesel & biomass feedstocks:
477–489. review & analysis of the biochemistry, energetics & economics. Energy Environ. Sci. 3,
Milledge, J.J., 2011. Commercial application of microalgae other than as biofuels: a brief 554–590.