Renewable and Sustainable Energy Reviews 71 (2017) 954–958

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Renewable and Sustainable Energy Reviews

journal homepage: www.elsevier.com/locate/rser

Solar energy conserved in biomass: Sustainable bioenergy use and MARK

reduction of land use change
⁎
Niclas S. Bentsena, , Ian M. Møllerb
a
University of Copenhagen, Department of Geosciences and Natural Resource Management, Rolighedsvej 23, DK-1958 Frederiksberg C, Denmark
b
Aarhus University, Department of Molecular Biology and Genetics, Forsøgsvej 1, DK-4200 Slagelse, Denmark

A R T I C L E I N F O A BS T RAC T

Keywords: Climate change mitigation requires a shift from fossil energy resources to renewables, and bioenergy crops are
Sustainability considered one of the major potential resources. At the same time future energy supplies are expected to be
Bioenergy sustainable, but the sustainability of energy crop production is challenged by concerns over its potential
Energy crops competition for arable land and disruption of food and feed markets. Protein in plant biomass is a challenge for
Protein conservation
sustainability, but also an opportunity. The challenge with protein is a disproportionately large land use foot
Land use change
print associated with its biosynthesis. Bioenergy exploits solar energy temporarily stored in biomass compounds
such as carbohydrate, lipid, lignin, protein and organic acids. Here we review energy cost estimates for
photosynthesis and growth and maintenance respiration and show – by comparing energy costs with the
amount of energy stored in different plant compounds – that protein conservation could improve the
sustainability of energy crop production by reducing land use impacts. The opportunity with protein in plant
biomass comes from the fact that favored energy crops like switch grass, reed grass and Miscanthus are
excellent protein producers on par with soybean and other protein-rich crops. Due to the scale of potential
future bioenergy deployment we find that energy strategies involving large amounts of herbaceous energy crops
will not be sustainable unless the proteins are conserved in some way.

1. Introduction assessment report [5] outlined bioenergy use by 2100 to be up to

It is commonly agreed that the combat against climate change
requires a fundamental change in the way energy is produced with a
shift from fossil energy resources to renewables. Currently (2014)
biomass contributes with 58.5 EJ to the global primary energy
consumption [1] and is by far the largest renewable energy resource.
Most, if not all, of the more comprehensive global energy projections
predict bioenergy to play a significant and increasing role in the future
energy supply. To meet the Sustainable Energy for all (SE4All) target of
doubling the share of renewable energy in the global energy mix before
2030, the International Renewable Energy Agency (IRENA), estimates
108 EJ yr−1 of biomass to be used by 2030 [2]. The International
Energy Agency (IEA) estimates in their World Energy Outlook [3]
bioenergy use to increase by approximately 40% between 2011 and
2035. The Global Energy Assessment [4] stipulates significant growth
in bioenergy to 80–140 EJ by 2050 rising to ~220 EJ yr−1 by 2100,
including extensive use of agricultural residues and 2nd generation
bioenergy based on lignocellulosic material. Similarly the
Intergovernmental Panel on Climate Change (IPCC) in their 5th
200 EJ yr−1 depending on climate ambitions and chosen policy
instruments. Residue biomass from agriculture is abundantly produced
on global and regional scales [6]. The IPCC Special Report on
Renewable Energy assessed the technical potential of agricultural
residues to 15–70 EJ yr−1 by 2050 [7]. More recent estimates suggest
a technical potential of 13–30 EJ yr−1 by 2030 [2] and correspondingly
27–30 EJ yr−1 by 2050 [8]. Considering the many challenges in
accurately estimating agricultural residue resources [9,10] it can be
assumed that around 30 EJ yr−1 could be technically available for
future energy purposes. Forest residues make up another significant
bioenergy resource base [9,11] technically capable of supplying up to
35 EJ yr−1 [11]. Agricultural and forest residues are considered
insufficient to meet the increased demand for bioenergy [12].
Consequently energy crops i.e. crops grown dedicatedly on arable or
marginal land to supply energy, is considered a major resource in
bioenergy projections [7,9,11,13,14].
Reports have expressed concern over the use of biomass grown on
agricultural lands for energy purposes due to its potential displacement
of other production (food or feed) [15] or impact on carbon reservoirs

⁎
Corresponding author.
E-mail addresses: nb@ign.ku.dk (N.S. Bentsen), ian.max.moller@mbg.au.dk (I.M. Møller).

http://dx.doi.org/10.1016/j.rser.2016.12.124
Received 12 February 2016; Received in revised form 21 December 2016; Accepted 26 December 2016
Available online 04 January 2017
1364-0321/ © 2017 Elsevier Ltd. All rights reserved.
N.S. Bentsen, I.M. Møller Renewable and Sustainable Energy Reviews 71 (2017) 954–958

Table 1
Solar energy conserved in plant compounds. Solar energy input was estimated on the basis of substrate requirement for growth and maintenance respiration of plant compounds. Energy
content was calculated as the higher heating value (HHV) based on the mass fraction of carbon, hydrogen, oxygen and nitrogen in the compounds.

Plant compound Representative Representative molecular formulaa Respiration cost (g glucose (g compound)−1) Energy inputd (kJ
compound g−1)
Growtha Protein Solute gradient Total
turnoverb maintenancec

Carbohydrate Monomer C6H12O6 1.00 0.43 1.43 261.9

Sucrose C12H22O11 1.05 0.43 1.48 271.6
Cellulose C6H10O5 1.11 0.43 1.54 282.3
Hemicellulose C11H18O9 1.12 0.43 1.55 284.3
Lipid Glyceryl trioleate C57H101O6 2.59 0.43 3.02 553.3
Lignin Coniferyl alcohol C10H12O3 1.92 0.43 2.35 429.7
Protein Zein C4.6H7.0N1.0O1.4S0.02 2.08 3.04 0.43 5.55 1016.8
Organic acid Citric acid C6H8O7 0.70 0.43 1.13 207.7

a
Based on McDermitt and Loomis [41].
b
Protein mass was assumed to increase linearly over the course of 150 days. The total protein turnover cost was calculated using a mean specific protein turnover cost of 40.5 mg
glucose per g protein per day [39].
c
The cost of maintaining solute gradients has been reported to make up approximately 20% of the total respiratory costs [39]. In this analysis the respiration cost was calculated on
the basis of a typical composition of Switch grass [42].
d
Energy input was found by multiplying the total respiration cost, expressed in g glucose, by 183.2 kJ g−1 glucose, the theoretical minimum solar energy requirement for glucose
synthesis [36].

in soil and biomass [16]. Replacing one cropping system with another
incurs a direct land use change (dLUC), which may influence the state
of agricultural lands in terms of soil carbon accumulation [17–21],
water use [22–25], nutrient availability [21,23] or soil erosion [26–29].
Another concern relates to market-mediated effects when either
cropping systems are changed or the use of crops is changed, e.g.
using corn for ethanol production instead of for food or feed. Market
mechanisms compensate for the changes in demand by encouraging
intensified production or agriculture expanding into undeveloped lands
(iLUC) [30–32] which is a serious threat to remaining forests
particularly in developing countries [33]. iLUC is likely to lead to
increased greenhouse gas emissions from bioenergy production
[16,34], and thus offset one of the potential benefits of using bioenergy.
Bioenergy has strong potentials to ensure local supply security and
to contribute to climate change mitigation [7,35]. Supplying bioenergy
sustainably and in the stipulated amounts, however, requires a new
perspective on intelligent use of biomass. Here we review early cost
estimates for growth and maintenance respiration of plant compounds,
and relate those to land requirements and land use change issues for
bioenergy production, and show that energy crop production fails to
meet sustainability intentions included in most renewable energy
policies unless valuable proteins in the biomass somehow is conserved.
2. Material and methods
2.1. Photosynthesis
Bioenergy essentially exploits solar energy conserved in biomass
and requires partial or complete decomposition of the biomass or its
individual compounds to release the conserved energy. Plant matter
primarily is made up of carbohydrate, lipid, lignin, protein and organic
acids in various proportions. Synthesis of these individual compounds
requires energy and substrate in the form of ATP, NADH and primary
photosynthates. In C4 plants, such as sugarcane, corn, switchgrass or
Miscanthus, the theoretical conversion efficiency of solar radiation to
glucose is 8.5% [36]. When the enthalpy of glucose is 15.57 kJ g−1 [37]
synthesis of 1 g of glucose requires a minimum of 183.2 kJ of absorbed
solar radiation.
2.2. Growth and maintenance respiration
Respiration has been divided phenomenologically into growth
respiration and maintenance respiration [38] although a three-part
division has later appeared [39]. Biomass production requires input of
carbohydrates to generate the energy carriers, ATP and NADH and to
provide carbon skeletons for the biosynthesis of more structured plant
compounds [38,40]. Growth respiration of carbohydrates provides the
carbon skeletons and the reducing power required for biosynthesis as
plant compounds generally are more reduced than carbohydrates [39].
Plant compounds can be characterized as biosynthetically ‘cheap’ to
produce (polymeric carbohydrate and organic acids) or ‘expensive’
(lipid, lignin and protein), and the amount of growth respiration
required to synthesize 1 g of different compounds varies almost four-
fold (Table 1). We here used glyceryl trioleate, coniferyl alcohol, zein
and citric acid as representative storage lipid, lignin monomer, cereal
storage protein and common organic acid, respectively.
Maintenance respiration provides energy for repair and mainte-
nance of biomass compounds. It is thought that a major part of the
energy cost for maintenance is associated with protein turnover and the
maintenance of solute gradients across cell membranes [39]. As such,
maintenance and turnover of protein adds considerably to the energy
cost of maintenance respiration.
3. Results and discussion
The overall theoretical efficiency of C3 and C4 plant production
(photosynthesis + respiration) is 4.6% and 6.0% respectively, when
estimated at 30 °C and the present atmospheric CO2 concentration of
387 ppm [36]. This is why C4 grasses such as Miscanthus and sugar
cane are considered to be the best energy crops. However, at lower
temperatures, such as those prevalent in Northern Europe, the
advantage of C4 plants is reduced [36,43]. A high-yielding C3 crop
like sugar beet, where the sugar is the primary product and the biofuel
in the form of waste biomass is a bonus, becomes very competitive
under these conditions with a productivity almost on level with sugar
cane [44].
The theoretical efficiency covers a considerable range of conversion
efficiencies between individual plant compounds as reported in several
studies [38,40,41,45]. McDermitt and Loomis [41] found that the
energy content of biomass compounds correlates well with the amount
of energy required to synthesize the compound. Their analysis did not
consider energy spent on maintenance respiration (protein turnover
and solute gradient maintenance). Including maintenance respiration
in the analysis shows that protein differs significantly from other
compounds in terms of energy return on investment (Fig. 1).

955
N.S. Bentsen, I.M. Møller
Fig. 1. Relation between solar energy required for biosynthesis and energy content of
plant compounds. Solar energy input is based on Table 1, column 8. Higher heating value
of plant compounds is approximated via the mass fraction of carbon, hydrogen and
nitrogen as HHV =3.75*[C]2–232*[C]–2230*[H] +51.2*[C]*[H] +131*[N] +20600,
based on Friedel et al. [46]. The line and shaded area indicate for all plant components
except Zein respectively linear fit and 95% confidence interval for individual predicted
values.
3.1. Respiration cost
Early cost estimates [38,41], which are still used, were based on the
theoretical ATP yields in the respiratory chain of animal mitochondria,
i.e. 3 ATP per NADH and 2 ATP per succinate, but we now know that
they are considerably lower especially in plants [47–49]. More
importantly, the respiratory chain of plant mitochondria contain
several alternative enzymes, which reduce the ATP yield substantially,
when used [48]. The consequence is that the cost estimates (calculated
in mg glucose) will be increased and the energy yield estimates
decreased to an unknown, but probably equal, extent for all processes.
Unknown because we do not know how much these alternative
enzymes are used during the life cycle of a plant, but they are more
active during biotic and abiotic stress [39,49], and when the plants
obtain their nitrogen as ammonium [50].
Since as much as 30–60% of all photosynthetically fixed carbon is
lost due to respiration [51] the selection of lines with lower respiratory
rates might be expected to give higher yields. In agreement with this, a
negative correlation has been observed between leaf respiration,
measured under optimal conditions, and yield for maize [52] and
ryegrass [53,54]. In spite of this, Kraus and Lambers [55] concluded
that “selection for low rates of mature leaf respiration is not an
appropriate method to select for high-yielding cultivars in perennial
grasses”. The explanation was that respiration, measured under
optimal conditions, did not reflect the true contribution to plant
respiration by the energy-wasteful enzymes (mentioned above), which
were activated to different extent in the cultivars under stress condi-
tions [55]. Attempts to create higher-yielding cultivars by knocking out
the genes encoding the energy-wasteful respiratory enzymes will
therefore most likely give plants that grow very poorly under field
conditions.
The effect of climate change on plant respiration should also be
considered. Higher temperatures combined with shortage of water will
favor C4 crops, while increased CO2 should favor C3 crops [48].
Increasing CO2 concentration and increasing temperature may both
stimulate respiration [56,57], but the effect of CO2 is still controversial
[58] and we do not know much about the effect on the energy
conversion efficiency and yield. This calls for further investigation.
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Renewable and Sustainable Energy Reviews 71 (2017) 954–958
3.2. Land use foot print
The ratio between energy content of individual plant compounds
and the energy required for their growth and maintenance translates
directly into a land use footprint as the energy input from solar
radiation is remarkably constant [59]. The more solar energy required,
the more land is needed. For equal amounts of energy stored in
biomass compounds, biosynthesis of protein requires 2–3 times as
much land for synthesis as other plant compounds, and the land use
foot-print of bioenergy and instigated iLUC may increase significantly
when plant proteins enter the energy pathway. Consequently land use
change impacts can be reduced by saving the proteins for other uses,
e.g. food supplement, and the growing pressure on arable lands from
increased demands for food, feed and energy [33] can be partially
alleviated.
The direct component of land use foot prints depends on land
productivity, which varies across crop species and varieties. Protein-
rich crops like soybean, as well as oil crops (except oil palm) tend to be
less productive than e.g. a number of lignocellulosic energy crops and
sugar crops [44]. The indirect component of land use foot prints
depends both on land productivity, market responses and trade
patterns [31,60]. Lapola et al. [16] investigated direct and indirect
land use change associated with meeting Brazil's 2020 biofuel targets
with sugar cane ethanol and palm oil biodiesel, and found that indirect
land use change effects overcome fossil fuel savings in the short to
medium term time perspective. Similar findings are reported by Holly
et al. [61]. Lapola et al. [16] also showed that indirect land use change
effects contribute far more to greenhouse gas (GHG) emissions than
direct effects. Similar result was shown for cellulosic biofuels in USA
[34]. A review by Wicke et al. [62] demonstrated the large variability in
land-use-change-related GHG emissions from 1st generation biofuels;
reports on corn ethanol show GHG emissions between −60 and +100 g
CO2eq MJ−1 fuel. Corresponding numbers for wheat ethanol fall
between −80 and +25 g CO2eq MJ−1 fuel. The large variability in
reported land-use-change-related GHG emissions can be attributed to
the context-specific nature of land use change, but also that the
methodology for estimating particularly iLUC impacts has not been
fully developed [62–66]. Strategies to mitigate land use change effects
includes e.g. increased crop productivity, increased efficiency of
bioenergy supply chains, minimization of land degradation and inte-
gration of food, feed and fuel production [62]. In line with the latter
strategy this review suggests a technological solution to increased
integration (see Section 3.3).
3.3. Perspective and conclusions
Using plant protein for energy generation may seem speculative,
but it actually takes place on a large scale. In 2013 more than 1.1
million ha of arable land in Germany was allocated to energy crops for
biogas [67]. Corn and sugar beet are preferred crops and the proteins
(5–10% of dry matter content) in the feedstock are destroyed during
digestion. The Global Energy Assessment [68] report a potential of 88
EJ of lignocellulosic energy crops by 2050. This corresponds to
approximately 4.5×109 t dry matter, and lignocellulosic crops favored
for bioenergy like switch grass, Miscanthus and reed grass [35,69–72]
contain 5–15% protein (dry weight basis) depending on species and
time of harvest [42,73–75]. Using this amount of grassy energy crops
potentially destroy approximately 0.45×109 t protein. For comparison,
according to the FAO [76], the world cereal production in 2014 was
2.8×109 t (fresh weight) of which 10–12% (dry weight basis) [77] is
protein corresponding to approximately 0.25–0.30×109 t. Cereals
covered 721×106 ha in 2014 [76].
The scale of potential future energy crop deployment calls for
attention to protein conservation, either through conversion technol-
N.S. Bentsen, I.M. Møller
ogies that do not destroy proteins or through protein separation prior
to conversion. Protein conservation is not without challenges; it adds
complexity, cost and energy consumption to conversion processes.
Alternatively it limits the choice of conversion pathways.
Thermo-chemical conversion of biomass is favored for largescale
use of bioenergy because of flexibility and the ability to convert a large
fraction of the carbon in biomass feedstock into various fuels and
products [78,79]. On the other hand thermo-chemical conversion
destroys all compounds in the feedstock, also proteins. Some bio-
chemical conversion pathways conserve proteins, e.g. some forms of
fermentation to ethanol [80], while anaerobic digestion to biogas
destroys proteins.
Biomass separation prior to energy conversion can save part of the
proteins in bioenergy feedstock. More than 80% of the proteins present
in the feedstock can ideally be extracted [73] chemically or mechani-
cally. Bals & Dale [75] model a number of mechanical and chemical
extraction scenarios and report extraction rates of 40–60% applying
standard technology, and also that protein extraction in most cases can
be done with a net profit.
Leaf protein extraction has been discussed since the 1940s and later
also the opportunity for combining bioenergy and protein production
with various grass crops [73]. Grassy energy crops are excellent protein
producers on par with e.g. soybean due to much higher total biomass
production. In extracting protein prior to energy conversion a limited
amount of bioenergy potential is lost. Less than 10% of the total energy
output is attributable to protein [74]. This loss is offset by reduced land
use impacts affected by protein's disproportionately large land use foot-
print associated with its biosynthesis.
As described above land use foot prints (dLUC + iLUC) of energy crop
production are context specific, but conserving 50% of the proteins from
88 EJ of grassy energy crops would yield the same amount of protein as
approximately 600*106 ha of world average cereals. The potential for
alleviating the increased pressure on land as well as improving the
sustainability of energy crop production is clearly very significant.
Acknowledgements
We thank Hanne Nina Rasmussen and Poul Erik Jensen, both
University of Copenhagen, for valuable comments and suggestions to
the manuscript. The research presented here is part of the
BIORESOURCE project funded by the Danish Council for Strategic
Research grant no. 11–116725 to NSB. IMM is supported by grants
from the Danish Council for Independent Research – Natural Sciences
and Danish Council for Independent Research – Technology and
Production.
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