Bioresource Technology 245 (2017) 162–170

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Bioresource Technology
journal homepage: www.elsevier.com/locate/biortech

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
a
German Institute of Food Technologies – DIL e.V., Prof.-von-Klitzing-Str. 7, 49610 Quakenbrueck, Germany
b
Institute for Food and Environmental Research (ILU) e.V., Arthur-Scheunert-Allee 40/41, Nuthetal, Germany
c
Sustainable Chemistry (Resource Efficiency), Institute of Sustainable and Environmental Chemistry, Leuphana University of Lüneburg, Scharnhorststr. 1, C13.203, 21335
Lüneburg, Germany

A R T I C L E I N F O A B S T R A C T

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

⁎
Corresponding author.
E-mail address: s.smetana@dil-ev.de (S. Smetana).

http://dx.doi.org/10.1016/j.biortech.2017.08.113
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.
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,
microalgae (as a source of proteins) are known to represent beneficial
nutritional qualities (Spolaore et al., 2006), but economic and en-
vironmental benefits of their production are questionable. That is why
life cycle assessment (LCA) of microalgae-based products and their
comparison with more traditional protein foods is the main purpose of
this study. Additionally, the results of the LCA should provide an insight
on the use of microalgae for feed purposes.
This article focused on LCA of microalgae and cyanobacteria (fur-
ther microalgae) application for food and feed purposes, based on
models for pilot industrial scale of cultivation and processing. It high-
lights a few main issues associated with comparability of technologies
and their upscaling issues in upstream and downstream production
processes. Multiple microalgae species, variations in their cultivation
and processing make the sustainability assessment challenging and not
always reliable due to the variations in scales and approaches. The goal
of the research is the systematic LCA of generic microalgae production
(with two model species: Chlorella vulgaris and Arthrospira platensis) for
food and feed products. Additional points of the article would touch the
environmental improvement potential of alternative strains cultivation
(Chlorella pyrenoidosa), use of different feeds and resource inputs and
further processing (high-moisture extruded products, extracted oils and
protein meals). The outcomes of the article indicating the most pro-
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. Methods and materials
2.1. Life cycle assessment
2.1.1. Goal and scope of the study
The goal of the study was to perform a LCA of different ways of
microalgae production and processing at industrial pilot scale and
compare the results with traditional benchmark products (food and
feed). The results were expected to provide and answer on the claims of
better environmental sustainability of microalgae use for food and feed
purposes. Such approach required the setting of a proper functional unit
(FU), system boundaries and assurance of data quality. FUs considered
in the study included the modelling of microalgae production facilities
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Bioresource Technology 245 (2017) 162–170
of the same production level (a step missing in many LCA of microalgae
production in literature). Moreover, FU considered variations in the
properties of harvested microalgae biomass and further produced food
and feed. The inclusion of such variations of microalgae production and
processing allowed to cover the scope “from cradle to processing gate”
with system expansion to the potential by-product generation and/or
waste treatment at cultivation and processing stages.
The presented LCA was divided into four main parts: (1) modelling
and analysis of microalgae production under autotrophic and hetero-
trophic conditions at the same production scale; (2) processing of the
microalgae biomass into food and feed suitable products; (3) compar-
ison of microalgae-based food and feed products with more traditional
benchmarks; and (4) sensitivity analysis and identification of more
sustainable scenarios of microalgae production. The assessment fol-
lowed the standard LCA approach (ISO, 2006a,b) and used professional
SimaPro8 software and adapted ecoinvent 3.1 datasets for background
data (electricity and water supply, heat generation, etc.). At the same
time, the study relied on the simultaneous use of two midpoint impact
assessment methods (ReCiPe V1.08 and IMPACT 2002+) (Goedkoop
et al., 2013; Jolliet et al., 2003) to get the possible variation ranges of
main midpoint characterization factors and exclude the limitations of
both methods. For the integrated results interpretation, the study based
on the similar endpoint impact assessment methodologies.
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-
lished and innovative options of microalgae cultivation. The potential
impact of food system transformation due to the microalgae production
(consequential approach) was not considered. However, the study fol-
lowed a “prospective attributional approach” (Hospido et al., 2010)
aiming to indicate the advantages (or disadvantages) of microalgae-
based food and feed in comparison with traditional alternatives pro-
duced via current state technologies and compared to different steady
states (without possible future implications included). Attributional
approach in LCA required allocation of environmental impact between
microalgae biomass products (oil and proteins), which was performed
according to economic values. System expansion was applied to the
scenarios of waste and side-streams application as microalgae nutrition
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
Outputs
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
Outputs
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
Outputs
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

Outputs
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

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

164
S. Smetana et al.
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
The study included five initial scenarios for the cultivation of mi-
croalgae (two species and three cultivation methods, with exclusion of
heterotrophic cultivation of A. platensis due to the low efficiency of
production). In order to reflect the variety of selected processing
methods for food and feed, three main resulting products were included
(whole dried microalgae powder, high-moisture extruded product and
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
like a part of sensitivity analysis. Such approach allowed the estimation
of influence of system boundaries, FUs and allocation rules (Fig. 1).
Sensitivity analysis, aimed for the optimization of microalgae produc-
tion, included additional scenarios: consideration of microalgae Chlor-
ella pyrenoidosa, selection of energy sources and change of processing,
feeding substances, and climate conditions.
2.3. Data sources
The study relied on several sources used for the cultivation model
construction. From one side the relevant literature sources on the cul-
tivation of Chlorella and Spirulina in specific conditions (Bux and Chisti,
2016; De Visser et al., 2014; Li et al., 2007; Perez-Garcia and Bashan,
2015; Schipperus et al., 2014; White et al., 2015) were considered.
From the other side LCA models were supported with data on lab scale
cultivation of Chlorella from Institute of Sustainable and Environmental
Chemistry (Leuphana University of Lüneburg, Lüneburg, Germany) and
pilot scale cultivation and processing of Spirulina from Institute for Food
and Environmental Research (ILU e.V.; Nuthetal, Germany). Fore-
ground data of microalgae biomass processing was partially collected
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Bioresource Technology 245 (2017) 162–170
during processing trials in German Institute of Food Technologies (DIL
e.V.; Quakenbrueck, Germany) and in Institute for Food and Environ-
mental Research (ILU e.V.; Nuthetal, Germany) and partially from lit-
erature sources (Brentner et al., 2011; Bux and Chisti, 2016; Handler
et al., 2014, 2012; Vandamme et al., 2013). Background data on pro-
duction of resources (electricity, heat, fertilizers), as well as the agri-
cultural stage of alternative feeds were based on data from ecoinvent
3.1 (Zurich, Switzerland) adapted to the study conditions (Table 1).
2.4. Assumptions
The study relied on a number of conclusions made based on current
scientific literature and personal communications with experts in the
field. It was assumed that the microalgae production in all three sce-
narios took place in Berlin, Germany. Such an assumption resulted in
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
of energy mix typical for Germany (ecoinvent 3 database) for the
consideration of electricity use. The main sources of carbon consisted of
atmosphere air with addition of concentrated CO2 for ORP and TBR
scenarios and glucose (sugar beet production) for HTF scenario.
Initial cultivation of seed microalgae media was excluded from
model scenarios due to the minor role and impact. Processing of mi-
croalgae biomass included a few stages. First microalgae media un-
derwent electrical flocculation (was selected to provide a high-quality
biomass suitable for food purposes) and centrifugation, which allowed
to eliminate extra moisture and recycle it (ORP and TBR scenarios).
Further processing included lyophilisation (freeze-drying) and fractio-
nation (separation of oil from dry powder biomass). Microalgae pro-
cessing models also enclosed assumption for the downtime and losses in
S. Smetana et al.
microalgae cultivation due to technical failures and cleaning proce-
dures. Cleaning procedures in TBR scenarios consisted of treatment via
3% hydrogen peroxide and 0.5% citric acid, HTF scenarios excluded
treatment with citric acid but and additionally relied on sterilization
with steam. Fractionation (separation of oil and protein biomass) con-
sisted of bed milling and supercritical CO2 extraction (Brentner et al.,
2011).
3. Results and discussion
3.1. Cultivation of biomass
Most of the scenarios of microalgae biomass cultivation relied on
the similar scale of production. According to the studies (De Visser
et al., 2014; Li et al., 2007; Schipperus et al., 2014) it was estimated
that the functioning of ORP with a volume of 300 m3, PBR – of 25 m3
and HTF – of 2.5 m3 would provide the similar amount of biomass
(1.4–1.8 ton dry matter year−1). Owning the low efficiency of A. pla-
tensis production in heterotrophic conditions, relevant scenario was
excluded from LCA. Among the other scenarios (Fig. 2) the highest
environmental impact was indicated for the microalgae production via
ORP for both species (7.7–9.7 mPt). TBR scenarios had impact in the
range of 4–4.7 mPt with more beneficial results for A. platensis. The
least environmentally impacting scenario was heterotrophic cultivation
of C. vulgaris with overall environmental impact of 0.4 mPt.
The highest impact was indicated for categories of non-renewable
energy consumption, global warming and respiratory inorganics emis-
sions. The impacts were associated with cultivation of microalgae (for
scenarios CORP and SORP) and with cleaning procedures (for scenarios
CTBR and STBR). Scenario CHTF was characterized with impacts gen-
erated using glucose and electricity for cultivation. Therefore, the
limitation of microalgae production as a viable source of protein bio-
mass was connected with the low concentration of microalgae in high
volumes of water, which should be kept in a constant dynamic state,
cooled or warmed due to the changing environmental conditions.
3.2. Protein powder concentrates
The cultivation of microalgae included flocculation and cen-
trifugation in order to get concentrated fresh biomass “soup” or fresh
biomass reviewed in previous chapter. The simplest further processing
and application for food purposes included drying of the biomass to the
state of powder. In order to preserve the valuable components of mi-
croalgae cells (e.g. proteins) the study did not rely on common thermal
methods (spray, oven or drum drying). Instead, gentler and nutrient
preserving lyophilisation (freeze-drying) was considered for protein
powders production from whole microalgae in current study. The sen-
sitivity analysis included verification of the method change for relevant
scenarios.
The distribution of results (Fig. 3) for FU of 1 kg of protein powder
concentrate (4% moisture content) were similar to the results of fresh
biomass comparison (Fig. 2). The protein powder concentrates pro-
duced via OPR scenarios had higher impact comparing to the scenarios
based on TBR or HTF (Chlorella only). Such results were logical due to
similar technological process of fresh biomass processing into dry
protein powder.
High energy consumption rates in CORP and SORP scenarios were
related to the need of maintaining of stable temperature conditions
throughout a year. It included the need to warm up ORP and TBR in
winter months and cool them down in summer and to mix the fluid in
the systems. Such results indicated environmental “hotspots”, asso-
ciated with the need to select optimal climate conditions for cultivation
of systems, which requite high volumes of water for the production. At
the same time, the processing of the biomass was responsible for 5–10%
of environmental impact only. Even though, many literature sources
indicate high energy requirements for microalgae processing (Brentner
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Bioresource Technology 245 (2017) 162–170
et al., 2011; Handler et al., 2014; Vandamme et al., 2013), these im-
pacts were of a relatively low importance in this study.
The comparison of environmental impacts of whole microalgae
protein powder modelled in current study with more traditional protein
concentrates used for food and feed (Table 2) indicated that ORP and
PBR scenarios were more environmentally impacting than most tradi-
tional sources. However, they were in the same range of impact in ca-
tegories of freshwater depletion and land use. CHTF scenario despite
being the most environmentally promising way to produce microalgae
in conditions of Germany (Berlin), still had relatively high impacts in
categories of land use, energy use and global warming potential (con-
nected to glucose use as a source of carbon). Such results indicated that
use of microalgae as food protein powder concentrate was not more
environmentally friendly than vegetable sources and in the same range
of impact as animal derived sources of proteins. Therefore, the en-
vironmental sustainability of microalgae protein powders should not be
claimed without justification.
3.3. Extracted protein and oil-based products
Microalgae are commonly used for the production of oil for biofuel
purposes and protein biomass for food and feed (Shi et al., 2017). At the
same time, microalgae are considered as a source of valuable bioactive
compounds (e.g. pigments, vitamins, enzymes) and multiple production
and extraction methods are developed (Chew et al., 2017; Matos et al.,
2017). That is why current study identified potential environmental
benefits of extracted oil and bulk proteins from microalgae (according
to the identified microalgae production scenarios). They were perceived
as raw components further applicable for various purposes (functional
foods, nutraceuticals, and biofuel).
The comparison results (Fig. 4) identified that the differentiation of
environmental impacts became more evident for oils (scenarios with C.
vulgaris had higher environmental impact) while for protein meals
concentrates the difference between species was negligible. It was
connected with environmental impact allocation due to a higher price
of microalgae oil than protein meal (used as feed in most cases).
However, further extraction of specific high-value protein components
could change the allocation rules if economic conditions were con-
sidered (possibility for further studies).
3.4. Moisturized protein products
Another potential use of whole dried microalgae protein powder
includes its use as a component of more complex food products. For
example, high-moisture extrusion incorporates mixing of the compo-
nents (powder and water), dynamic cooking under increased pressure
and temperature conditions (up to 170 °C) with further cooling in a
cooling dye, which allows forming a fiber meat-like texture of a pro-
duct. High-moisture extrudates (HME) are also characterized with the
main nutritional properties similar to those in meat. Dried whole A.
platensis was tested for the ability to be used as a raw component for the
extrusion in DIL e.V. (Quakenbrueck, Germany), where it was possible
to reach the rate of inclusion from 30% (in combination with soya
protein concentrate) to 75% (in combination with soya protein con-
centrate and carrageenan) (DIL e.V., personal communication). The
development of high-moisture extruded meat substitutes based on au-
totrophic microalgae biomass resulted in green-colored products which
had higher environmental impacts than soy-based meat substitute, but
were comparable in environmental impact to meat (Fig. 5). Moreover,
meat substitutes based on soybean meal and heterotrophically pro-
duced Chlorella protein powder had lower environmental impact than
pork and chicken meat. These results were very promising as they in-
dicated that despite overall high inefficiency of the most common mi-
croalgae cultivation methods, there was a possibility for further im-
provements. It was not possible to recommend the use of microalgae
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
eq.)
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
concentrate
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
extrusion of meat substitutes could result in more environmentally
perspective food protein products.
3.5. Sensitivity analysis
Based on the results of LCA for the scenarios of the current study,
the sensitivity analysis concentrated on reviewing potentially more
optimized scenarios. They included heterotrophic production of C.
vulgaris fed on alternative to glucose source of carbon (26% of en-
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
80% of impact associated with heating); heterotrophic production of
alternative microalgae strain (C. pyrenoidosa) fed on alternative carbon
source – food waste composed of rice, noodles, meat and vegetable

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

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S. Smetana et al.
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-
croalgae has a potential of environmental impact reduction by 40%,
while the change of carbon source could reduce the impact by 25–40%.
The most promising scenario in this case would be the combination of
microalgae production in heterotrophic conditions with the use of food
waste as a source of carbon and photovoltaic energy generation for
cultivation. Such scenario would result in the production of protein
concentrate powder, which would have an integrated environmental
impact of 0.98 mPt for 1 kg (GWP: 2.25 kg CO2 eq., ED: 28.4 MJ, LU:
0.31 m2a) and would be one of the most beneficial protein sources
(Table 2). This final result of LCA modelling indicated the re-
commended path for further research and innovation activities, aiming
to create a more sustainable system of alternative protein sources
production.
4. Conclusion
Pilot industrial scale (1.4–1.8 ton dry matter year−1) of A. platensis
and C. vulgaris production with autotrophic (open raceway pond, tub-
ular photobioreactor) and heterotrophic (fermenter) systems had
higher environmental impacts than production of most traditional food
and feed protein sources. High impacts related to heat and energy use
(autotrophic cultivation) and glucose for microalgae feed (hetero-
trophic). Heterotrophic cultivated protein biomass applied for high-
moisture extrusion products was more beneficial than pork and beef.
Further optimization of production with C. pyrenoidosa on hydrolyzed
food waste could provide more beneficial protein concentrate (2.25 kg
CO2eq., 28.4 MJ, 0.31 m2a per 1 kg).
Acknowledgements
This work was supported by Ministry for Science and Culture of
Lower Saxony (Vorab programme) and Volkswagen Foundation in the
scope of the project “Sustainability transitions in food production: al-
ternative protein sources in socio-technical perspective”. Additional
169
Bioresource Technology 245 (2017) 162–170
support was given by the German Ministry of Economics and Energy
(via AiF) and the FEI (Forschungskreis der Ernaehrungsindustrie e.V.,
Bonn), project AiF 129 EBG.
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