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Limitations and prospects of natural photosynthesis for bioenergy production

AWD Larkum
Solar energy is clearly a major future source of energy for humans. While solar photovoltaic and thermal harvesting are attractive there will be a need for biofuels to replace fossil fuels. Natural photosynthesis offers a means to do this, but photosynthesis is inherently inefcient. Terrestrial plants have already been used as a source of biofuels and this use will increase in the future, despite a number of attendant problems. Microalgae as a source of biofuels have to be technically proven and articial photosynthesis/biohydrogen production lies further into the future. Consideration of these approaches must be weighed against (i) crop production in a hungry, as well as a fuel-hungry, world and (ii) the need to sustain biodiversity.
Address School of Biological Sciences, Heydon-Laurence Building (A08), University of Sydney, NSW 2006, Australia Corresponding author: Larkum, AWD (alark@mail.usyd.edu.au)

future there are many possible avenues that hold out promise for a more sustainable world.

Solar energy input into the Earths atmosphere

Data on the amount of energy reaching the Earths outer atmosphere and penetrating to the surface have been available for many years [1,2]. A recent re-evaluation [3] has provided information by which insolation at any point on the Earth can be modelled to yield annual, seasonal, and daily values. Despite decadal variation [4], the annual value of total solar energy received at the Earths surface is $2,500,000 exajoules (EJ). Ignoring the near infra-red wavelengths that are not available to photosynthesis, we have approximately 2,200,000 EJ of the available energy per year. Perhaps surprisingly, on a cloudless day, the temperate zones offer good levels of solar energy, even though the season is shorter ([5], Table 1). Actual radiation levels can be obtained over 10, 20 or more years from various sources, e.g. ref [6].

Current Opinion in Biotechnology 2010, 21:271276 This review comes from a themed issue on Energy biotechnology Edited by Jan R van der Meer and Alexander Steinbuchel

World energy usage by humans

0958-1669/$ see front matter # 2010 Elsevier Ltd. All rights reserved. DOI 10.1016/j.copbio.2010.03.004

World energy use (values for 2005) is approximately 500 exajoules per year (EJ, or 5 1020 J yr1). Of this total, 8090% is derived from fossil fuels [6]. In equivalent units, this is an average consumption of 16 TW (1.6 1013 W). In comparison with 1980, this represented an approximate doubling of energy use over the previous 25 years. On the basis of the earths surface area of $510,000,000 km2 and the value of annual solar radiation (above) one can calculate that the worlds energy needs would be satised with an area of 1,150,925 km2 if 10% of the solar energy could be converted to useable energy [5], i.e. $0.02% of the total surface area or 0.07% of the land surface, i.e. equivalent to a country the size of Ethiopia, Egypt or Colombia. These then are the realistic values that we need to work with in considering solar energy conversion into organic products by cyanobacteria, algae and plants.

Introduction
Oxygenic photosynthesis occurs in cyanobacteria and their eukaryotic successors, algae and land plants and is summarised by the equation CO2 H2 O light energy ! CH2 O O2 (where the parenthesis around CH2O is a reminder that this is only a portion of an organic molecule, in this case a sugar molecule; and the energy required is 480 kJ per mole of CO2)[1,2]. This process is the major route for solar energy conversion on the Earth today and is carried out by cyanobacteria, algae and plants. Other inputs of organic energy into the biosphere (chemical, thermal, etc) are by comparison negligible. So in looking for future replacement of fossil fuels, harnessing solar energy in photosynthesis, either natural or articial, is an attractive option, since there are vast amounts of unused solar radiation. On the negative side, this option has serious problems with efciency, carbon footprint and in its conict with growing food for a hungry world. Nevertheless in the
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Solar energy conversion by cyanobacteria, algae and plants

In theory energy conversion by algae and plants may be as high as $11% in the initial stages of photosynthesis [7,8], but this considers only the initial conversion into organic compounds and not secondary processing, growth, etc. Calculations of long-term theoretical solar energy converCurrent Opinion in Biotechnology 2010, 21:271276

272 Energy biotechnology

Table 1 Budget for solar energy at various sites on the Earths surface and theoretical primary productivity at various latitudes. *Values for the tropic of capricorn and 37-S are similar. The values for daily carbon are for the summer solstice, the equinox and the winter solstice, except for the Equator where there is only one solstice. Taken from [3]. Latitude Equator Darwin (128280 S) Growing season All year (365 d) All year (365 d) Daily carbon xation (gC 2 1) 19.8 17.6 20.3 19.2 13.9 21.8 17.6 9.90 22.3 14.2 4.98 20.8 8.09 0.606 Total Irradiance (E m2) 20 238 19 710 Total Carbon Fixation (gC m2) 6 823 6 602

Tropic of Cancer* 238300 N

All year (365 d)

18 615

6 136

378N*

7 Months (214 d)

12 208

4 031

558N

5 Months (153 d)

8 130

2 533

sion into organic matter by plants and algae yield rates of 18 gC d1 (Table 1), which is an efciency of conversion of $3.2% (cf. [2,9,10]). However, the best solar energy conversion rates of agricultural plants, e.g. Napier grass and sugar cane, are much less than this, with a maximum of 1.6% [2,11,12] and these are the star performers grown under the most pampered conditions: the more usual rates for temperate crops and forests are 0.2 to 0.4%. It is true that only a part of the primary production gives rise to the crop (and only parts of the crop are used). Using all the aboveground parts could improve yields; and thus biomass production of biofuels has potential to improve yields, but probably not much more than, at maximum, a 2.5% conversion rate. This would leave below-ground parts largely unutilised. Cyanobacteria and algae have the further potential that in theory all the primary production could be utilised [10], but other factors mean that algae overall are little more efcient, and in terms of energy input much more costly [13] (also see Photosynthesis in air vs photosynthesis in water and Bioenergy from algal ponds and photobioreactors). Furthermore, in all these possibilities there are many hidden drawbacks, which have hindered realisation of high efciency of conversion, with the attendant burden of high input of energy, largely in the form of fossil fuels, and fertilisers (see, e.g. refs [10,14]). The low yields from plants, algae and cyanobacteria, is a constant frustration in comparison with physical methods of solar energy conversion such as solar photovoltaic cells. It is not likely that genetic engineering will greatly improve the efciency in the short to medium term, although small gains are possible. The major losses of photosynthesis can be put down to some major, as well as many smaller, inefciencies [2,7,8,13]: 1. Two photosystems (in series) rather than one.
Current Opinion in Biotechnology 2010, 21:271276

2. Dependence on a chlorophyll-based system that is dependent (in the greater part) on the spectrum of chlorophyll and on harvesting energy from the rstexcited singlet state of chlorophyll a. 3. Inefciencies of light-harvesting, levels of enzymes vs. changing light climates, and chemical inefciencies. 4. Photoinhibitory damage to photosystem II. To re-engineer natural photosynthesis to overcome these inefciencies will not be an easy challenge and has led to a move to biomimetics of photosynthesis, i.e. towards articial photosynthetic systems (see Hydrogen production and articial photosynthesis).

Photosynthesis in air vs photosynthesis in water: Land vs ponds and lakes vs the sea
Land plants have a hidden advantage over aquatic plants in that they have evolved homoiohydry to enable them to photosynthesise in air using leaves that have evolved to utilise the rapid diffusion of gases in air, which is of the order of 10,000 times faster than that in water [15,16,17,18]. Thus algae or cyanobacteria (in water) must either be limited by stirring and grow slowly - giving rise to a low rate of natural primary production - or be stirred and grow faster, which for algal ponds and photobioreactors means employing some form of mechanical stirring (see Bioenergy from algal ponds and photobiorectors). Primary production by phytoplankton in lakes or oceans is very low [9,11]. The major reasons for this are because (i) stirring in such waters is low, and (ii) levels of essential nutrients are also low. Nevertheless, the large areas involved and the essentially natural and free primary production might make this an attractive area for xedcarbon harvesting; however, the difculty of harvesting the product makes this is an unacceptable option, except for shallow ponds.
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Limitations and prospects of natural photosynthesis for bioenergy production Larkum 273

In shallow lagoons and ponds, especially those that are polluted, opportunities do exist [19]. Nevertheless the difculties of adapting new practices to shallow water bodies will certainly delay this use for a number of years. As a result, terrestrial plant bioenergy will be most used in the near future (see next section).

Bioenergy from plants

Agricultural and forestry production must sustain any approaches on land in the short to medium term. Two approaches have been promoted recently, i) a search for new crops that can produce biofuels [20], and ii) the use of trees and other lignocellulose-rich resources for biofuels [2124]. The use of new crops, such as switchgrass, jatropha and Miscanthus, may have advantages but the commercial viability has yet to be tested [2530]. The use of lignocellulose from grasses, trees and other plants is a promising way to produce biofuels but the technology has yet to be proved [31,32,33,34] and initial results have been slow and disappointing [35]. The alienation of land previously used to produce food has ethical challenges, but nevertheless is going ahead in a number of countries, such as the USA, Brazil and many East Asian countries [24,36,37,38,39,40,41,42,43,44,45, 46,47]. There are reliable reports that this move has already driven up the price of food [24,43,47,48,49] and is not sustainable [50]. As a result several analyses have looked at alternative sources of land. Grazing land could have potential, but this would conict with the production of meat [44]. Marginal land may have potential for new crops; it could also double up as sites for tree production [38]. Some estimates suggest that lignocellulose conversion alone could provide the majority of fuels in the future, although the solar and carbon footprints of such a proposal has yet to be costed and early analyses suggest that this approach is not sustainable [51] Other downsides may be in the form of land alienation, increased production of greenhouse gases, pollution and threats to biodiversity [45,46,50]. Biochar is yet another unproven technology favoured by some [52,53]. Finally, it has to be realised that, despite the need to plant more trees and other remedial measures, at present deforestation is a much more serious issue.

deserves. Other problems are photoinhibition and other stresses [56] decline in yields due to pathogens, ageing, etc, and optimising optical path lengths and the package effect, as well as the large scale nature of such projects if they are to meet the needs of bioenergy production [10]. Thus, while these systems present novel advantages over land-based agriculture and water-based mariculture, their potential must be thoroughly assessed and the disadvantages acknowledged. Theoretical yields are discussed in Solar energy conversion by cyanobacteria, algae and plants. There will be much debate for some time to come over the actual yield potentials from algae. This is because in single celled algae it should be possible to redeploy a greater fraction of absorbed solar energy into xed carbon compared with land plants with their stems and root systems. However, the culturing of algae brings with it another set of problems such as stirring, nutrient supply, optimisation of the light eld, optimisation of the growth conditions and protection from pathogens and nuisance weed algae. While these factors have been discussed for small-scale pilot plants by many workers in recent times [5662] there is no clear way forward. Another area of confusion is over what is a realistic cropping factor; and on this there is at present a wide range of opinion for algal pond and photobioreactors; but little good data. Small-scale facilities can be nurtured to yield impressive xed-carbon outputs. However, it remains to be proved that this can be done on a long-term basis at commercial levels of at least 1000 ha. Even then it must be shown that transport costs to the area can be economically viable. Finally, water in many regions may be a prime commodity and the requirement for large amounts of water for algal ponds or photobioreactors may be antithetical to the overall need to conserve water. In the short-term, the prospect for the use of algae to provide signicant amounts of organic carbon, to sustain the human need for bioenergy, is limited. In the longer term the possibilities should be explored, but they come at the cost of a high solar footprint (see below), a high carbon footprint and many unknowns [63]. Over the recent past there have been some notable failures in this challenging eld [64]. Initially it can be seen that small-scale success can be obtained by taking advantage of local circumstances. For example, heat, stirring and nutrients could be obtained from power stations. Coastal lagoons and other shallow water bodies could be advantageous for algal ponds. Initially these could be operated with little stirring and no nutrient input, and harvesting could be done by simple means. In the longer term solar photovoltaic or solar thermal assemblies could be used to provide much of the energy needed for the algal farms. Sewage and other efuents could be used to provide nutrients.
Current Opinion in Biotechnology 2010, 21:271276

Bioenergy from algal ponds and photobioreactors

As noted in photosynthesis in air vs photosynthesis in water, the major disadvantage to overcome with either algal ponds or photobioreactors is stirring, with a second major disadvantage the provision of nutrients at a sufcient level to maintain optimum growth. The issue of stirring, although dealt with briey in a few earlier studies [54,55] has not been treated with the seriousness it
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274 Energy biotechnology

Perhaps the brightest possibility as regards algae is the production of value-added products. The commercial production of beta-carotene [65] is a good example here. There are many other potential products from algae such as sugars, biopolymers, lipids and antibiotics. In negotiating the commercial output of these products, the algal biotechnology industry would learn much that could eventually be fed back into the system in the production of algal biofuels.

more if solar photovoltaic panels are contemplated to offset the high-energy needs of algal farms, the solar and carbon footprints greatly increase.

Hydrogen production and articial photosynthesis

The production of hydrogen by algae, through the presence of the enzyme hydrogenase, has been the focus of projects in a number of countries. The results point the way to improved production, but are still in a very early stage. Hydrogen is a tempting fuel because of the low carbon footprint. Whether future work will emphasise a biological route via direct solar conversion or will use fermentative methods, or electrohydrogenesis or will employ a hybrid system partly involving solar photovoltaics is still a matter of debate [6871]. Articial photosynthesis involves the mimicking of natural systems using specially designed pigments and redox systems. This area clearly has potential for the longterm, but direction and feasibility are not yet clear [72]. If photosynthesis could be redesigned to overcome the inherent inefciencies of natural photosynthesis very strong gains could result.

Solar footprint of bioenergy

Solar footprint is the amount of land required by each person (in a country or in the world) to supply the current energy need in solar equivalents. Denholm and Margolis [66] concluded that the solar electric footprint from solar photovoltaic panels is about 181 m2 per person in the United States. However when the energy cost of manufacturing the devices is included the area will be substantially larger. There have been no equivalent calculations for bioenergy from land plants or from algae. Since the latter are much less efcient than solar panels the solar footprint must be considerably larger and the total land required globally would be much larger than the size of Ethiopia, Egypt or Colombia as calculated for solar panels in Solar energy input into the Earths atmosphere. If natural vegetation or natural algal lagoons are harvested, then, to some extent, it may be argued that the footprint is low. Yet in all such proposals there are hidden costs [27,41,67]. For algal ponds or photobioreactors the solar footprint would be considerably increased by the need to supply a large amount of energy for stirring and to provide for the hidden energy costs of fertilisers, harvesting and transport.

Conclusions
Natural photosynthesis is an ancient process on the Earth that evolved under conditions where efciency was not a selection pressure. The most efcient photosynthetic organisms are land plants. Algae and cyanobacteria, living under light-limited conditions, are generally less efcient but offer possibilities in the future. The 12% efciency of plants, algae and cyanobacteria cannot compete with solar photovoltaic panels or solar thermal collectors. Nevertheless natural photosynthesis will become increasingly used for the production of biofuels and organic products in a world where these will increasingly come into short supply. It seems unlikely that algae and cyanobacteria will be used as a source of bioenergy. In the longer term photobiohydrogen production and articial photosynthesis hold out possibilities. In all these cases, high carbon footprints, land sequestration, loss of biodiversity and other problems must be addressed.

Carbon footprint of bioenergy and biofuels

The carbon footprint of bioenergy crops might seem to be good, since algae and plants take up CO2 in their production. However, bioenergy is a high-cost end product and requires much infrastructure, both in production and harvesting of the product. As a result the production of biofuels from crops, such as bioethanol from sugar cane/ sugar beet and oil from palm oil, or from forests, have been found to have a rather high carbon footprint [41,47,63,67]. Nevertheless, this approach has reached commercial levels and the economics and carbon accounting can be done with reasonable condence. For algae, despite the prospect for higher yields and higher crop turnover, no commercial scale production has yet been achieved and only crude economic and carbon assessments can be made. Currently predictions are not heartening [63,64]. Any production of bioenergy crops from algae will be energy and carbon intensive. For obvious reasons, it may be possible to site algal projects adjacent to coal-red power stations and use waste heat and CO2 to offset the energy and CO2 requirements of the algal installations. Overall, though, this is not a viable alternative if thousands of hectares are to be utilised. FurtherCurrent Opinion in Biotechnology 2010, 21:271276

References and recommended reading

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