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© 1999 Nature America Inc. • http://biotech.nature.

com

FEATURE

Can biotechnology move us


toward a sustainable society?
A case study of biodegradable polymer production from agricultural feedstocks
casts doubt on the premise that alternative biological processes always offer
environmental benefits over conventional manufacturing processes.
Tillman U. Gerngross
The sustainability of a society based on finite has traditionally been viewed in a negative Of the various alternative polymers devel-
fossil resources is the subject of ongoing sci- light. As a result, much effort has been dedi- oped to date, polyhydroxyalkanoates (PHAs),
entific and political debate. One aspect of cated to developing alternative plastic materi- a class of aliphatic microbial polyesters, have
this debate, besides exploring alternative als that are both biodegradable and produced been considered among the leading candi-
energy sources, is the challenge to provide from renewable resources, preferably of agri- dates to replace conventional plastics on a
chemical commodities (fuels, lubricants, cultural origin. large industrial scale2. Like their petrochemi-
adhesives, solvents, paints, materials, etc.) to cal counterparts, PHAs are moldable, water
© 1999 Nature America Inc. • http://biotech.nature.com

an advanced consumer society, without insoluble, thermoplastic polymers. The most


Corn
depleting nonrenewable resources. An common PHA, poly-3-hydroxybutyrate
approach that has recently gained popularity (PHB), is a stiff, high-melting-point aliphatic
advocates the use of biological (fermenta- polyester similar to many industrial poly-
A.
tion) processes to produce chemical com- olefins. Unlike polyolefins, however, PHAs
modities from agricultural feedstocks1. can be synthesized by microorganisms, which
Fueled by advances in the area of metabolic can produce and store the polymer in the form
engineering, an array of products, ranging of intracellular inclusions at levels exceeding
from polymers to polymer intermediates Starch 80% of the cell dry mass (see Fig. 1). These
and industrial dyes, can now be produced by B. microbial polymers can be made entirely from
fermentation. With numerous such biologi- Glucose
glucose in a fermentation process and, in
cal approaches currently under considera- addition to offering favorable material prop-
tion, it is pertinent to analyze whether the erties, are completely biodegradable. Thus,
proposed processes have the intended effect C. Fermentation
the replacement of conventional plastics with
of sparing nonrenewable resources and ben- PHAs has been promulgated as a desirable
efiting the environment. approach to solid-waste management and sus-
Fermentation-based processes offer intu- tainable polymer production3,4.
itive advantages, such as aqueous processing
environments, nontoxic waste, and most D. Washing and centrifugation A cradle-to-grave analysis
importantly the use of renewable, nonfossil Several factors contribute to the environmen-
feedstocks. In most cases, however, these ben- tal impact and the degree of sustainability of a
E. Cell lysis
efits have not been critically weighed against given product or material. In many instances,
an overall inventory of materials and energy however, environmental impact is the result,
required to generate a given product. This not of the product per se, but rather of the
article offers a side-by-side comparison of a consumption of raw materials and the release
biological versus a conventional petrochemi- F. Washing and centrifugation
of waste products generated during manufac-
cal plastic manufacturing process to illustrate ture. Thus, a “cradle-to-grave” analysis, which
the complexity of choices confronting society incorporates manufacturing practices, energy
G. Concentration and drying
and the commodity biotechnology industry input/output, and overall material flows, is a
in the coming years. good benchmark for assessing environmental
Polymer resin impact and sustainability5,6.
Bob Crimi
Weighing the alternatives Contrary to the widespread belief that
Much has been made of the environmental Figure 1. The analyzed multistep PHA PHAs are a sustainable alternative to polymer
shortcomings of conventional, fossil oil–based production process. (A) Growing and production, a surprisingly high latent energy
polymers, such as polyethylene, polypropy- harvesting corn. (B) Processing of corn to content is associated with their fermentative
lene, and polystyrene. While these polymers yield glucose. (C) Sterilizing the medium and production. By considering the utilities
conducting a fermentation process by which
offer good material properties at a low price, glucose is converted to PHA (note cells
required to make glucose from corn, it is pos-
their environmental impact and manufacture containing PHA polymer in the form of sible to estimate that a PHA fermentation
intracellular inclusions). (D) Recovering the process consumes 22% more steam, 19-fold
biomass containing the polymer and washing more electricity, and 7-fold more water than a
it by centrifugation. (E) Disrupting the cell wall
Tillman U. Gerngross is assistant professor of and releasing the polymer from the cells. (F)
conventional process for producing poly-
biochemical engineering, Thayer School of Washing the polymer by centrifugation. (G) styrene. While only polystyrene is directly
Engineering, Dartmouth College, Hanover, Drying the polymer slurry to a powder that can derived from fossil oil, both polystyrene and
NH 03755 (tillman@dartmouth.edu) be processed to a final consumer product. PHAs require energy in their manufacture. As

NATURE BIOTECHNOLOGY VOL 17 JUNE 1999 http://biotech.nature.com 541


© 1999 Nature America Inc. • http://biotech.nature.com

FEATURE

Table 1. Direct raw material require- Table 3. Energy requirement for fermentative production of PHA from glucose.
ments for the production of polystyrene
versus PHA. Energy requirement (per kg PHA)
Item Electricity (kWh) Steam (kg) Fossil fuel equivalenta (kg)
Raw material requirement
(per kg polymer) Fermentation
Media sterilization b None 0.45 0.02
Item Polystyrene PHA Agitationc 0.32 None 0.09
Aerationc 1.27 None 0.35
Glucose None 3.33 kga
Coolingd 0.76 None 0.21
Petroleum fractions 1.78 kgb None
Inorganic salts 20 gb 149 gc
Downstream
Water 4 Lb 26 Ld
Centrifugation and washinge 0.50 None 0.14
aThe yield of PHA on glucose in bacterial fermen-
High-pressure homogenizationf 1.97 None 0.54
tations is 30%. bPetroleum fractions serve as a Centrifugation and washinge 0.50 None 0.14
feedstock and as an energy source in the manu- Evaporationg None 0.33 0.02
facture of polystyrene. The production of 1 kg of Spray dryingh None 2.00 0.10
polystyrene requires a total of 2.26 kg of fossil
fuels, of which 0.48 kg can be directly assigned to Total 5.32 2.78 1.59
the production of steam and electricity. Of the
remaining 1.78 kg, which serve as feedstocks, a aAmount of fossil fuel (kg) consumed to generate the electricity and steam listed in the same row. In 1997,
fraction is recycled and also used as an energy the US average for producing 1 kWh of electrical power, from all power sources (including geothermal,
source. For details, see refs 5,6. cInorganic salts hydroelectric, nuclear, and alternative power generation), required the direct combustion of 0.272 kg of
are required for the fermentation process in the fossil resources (83% coal, 13% natural gas, and 3.5% petroleum)8. Thus, the conversion of electricity to
© 1999 Nature America Inc. • http://biotech.nature.com

form of potassium phosphate, sodium phosphate, fossil fuel equivalent was carried out as follows: electrical energy (kWh) ´ 0.272 (kg/kWh) = fossil fuel
ammonia, phosphoric acid, and trace elements18. equivalent (kg). The conversion of steam to fossil fuel equivalent was as follows: steam (kg) ´ heat of
In the subsequent energy analysis, only the ener- evaporation of water (2,400 kJ/kg) / heat of combustion of natural gas (47,219 kJ/kg) = fossil fuel equiva-
gy to produce ammonia is taken into account lent (kg). Calculation assumes 100% efficiency, the use of natural gas for steam generation, and no heat
(which is about 109 g/kg polymer). dWater is loss. bMedium is continuously sterilized to 143oC for 30 s; 68% of energy is recaptured through a heat
required to fill the fermenter and for four washes. It exchanger and used to pre-warm the incoming medium23. cAgitation and aeration for this type of aerobic
does not include cooling water, which is expected fermentation with very high cell densities is estimated to require 5 W/L of power input. Power, delivered
to be recycled through a chiller or a cooling tower. by mechanical agitation and compressed air, totals 1.59 kWh/kg of PHA 24. dCooling assumes the use of
a fully jacketed 114,000 L fermenter (height to diameter ratio of 3 to 1) that has additional cooling coils on
the inside, providing a total cooling area 266 m2 or 2.32 m2 per m3. Under the assumed production sched-
ule (a 48 h culture that yields 190 g/L of biomass), approximately 17.6 W/L or a total of 2 million J/s (ref.
Table 2. Energy required to produce raw 23) must be removed. Coolant is provided through cooling towers and chillers (coefficient of performance
materials for the production of PHA. of 5.0), which deliver about 48,700 kJ and 18,000 kJ of cooling per kWh input, respectively 22. eFor cen-
trifugation, see ref. 15. Energy input was reduced by 50% to reflect the energy savings from our higher
solids content. f For cell disruption, see ref. 15. gEvaporation is performed with a triple-effect evaporator.
Item Energy (kJ) required requirement A preconcentrated slurry containing 30% solids is concentrated to 50% solids. This step requires the
(kJ/per kg of raw material) evaporation of 1.33 kg of water and requires 0.33 kg of steam per kg PHA. hThe final polymer slurry is
spray dried to yield a powder of the polymer. The energy required for spray drying is generally about
Glucose 8,129a twice the amount of the water that has to be evaporated from the slurry. Thus, about 2 kg of steam are
Inorganic salts 30,135b required to remove 1 kg of water, leaving 1 kg of dry polymer powder.
Water 5.6c
aEnergy to produce 1.52 kg of corn grain (60%
starch) and process the grain to yield 1 kg of glu- duction consumes significantly more energy, based on corn, which is one of the more ener-
cose minus energy for coproducts (33% of corn releases more net greenhouse gases8, and gy-intensive agricultural crops. Corn produc-
milling energy). Calculation: 1.52 kg ´ 2,442 kJ/kg therefore is no more sustainable than conven- tion in the US accounts for about 44%, 44%,
(ref. 11) + 4417 kJ/kg (corn wet milling) = 8,129
kJ. The entire corn wet milling industry consumed tional petrochemical polymer production. and 55% of total fertilizer, insecticide, and
147 trillion kJ of energy by combusting externally herbicide use, respectively9. Several
purchased fossil fuels or buying external electri- The balance of power researchers have attempted to quantify the
cal power13. In the same year, a total of 33.66 mil-
lion tons of corn grain were processed19. Thus, By compiling an energy and feedstock inven- energy required to till, irrigate, fertilize, and
the average energy input can be estimated to be tory of a “theoretical” large-scale PHA harvest corn, estimating that the process con-
about 4,375 kJ/kg processed corn grain, and process and a conventional polystyrene sumes between 2,226 and 6,722 kJ per kilo-
therefore the production of 1 kg of dextrose from
1.52 kg of corn grain (starch content 60%) con- process, it is possible to determine the envi- gram of corn grain9–11. By incorporating pri-
sumes about 6,650 kJ (ref. 20). Of that energy, ronmental benefits of substituting a petro- mary energy usage patterns of US farms, this
33% (2,194.5 kJ) is reallocated to the production chemical process with a biological process. translates into the combustion of between 50
of coproducts (corn meal, etc.), leaving 4,417
kJ/kg for glucose. In addition, two engineering
Only a minor fraction (less than 4%) of and 160 kg of fossil fuels per ton of corn
firms (Nofsinger, Kansas City, MO, and Process crude oil is refined into intermediates that grain12.
Systems, Memphis, TN) active in the construction serve as feedstocks for the polymer industry Subsequent processing of the corn also
of corn wet mills were contacted to confirm these
estimates. We obtained values ranging from
(the rest being used for production of trans- involves energy expenditure. On transfer to a
3,718 kJ to 5,631 kJ for the production of 1 kg of portation fuels and heating oil). Analysis of wet mill, it must be fractionated and processed
glucose from corn grain. bEnergy to produce 1 kg the polystyrene production process reveals an to yield gluten meal, oil, starch, and sugars
ammonia, which is used in the fermentation to energy requirement that is equivalent to the (mainly glucose and fructose). In 1991, the
control pH and provide nitrogen21. cEnergy to filter
and pump water to point of use22. consumption of 1 kg of fossil oil for each kilo- average energy needed to process 1 kg of corn
gram of polystyrene6. In other words, the syn- grain was about 4,375 kJ (see Table 2), which
thesis of 1 kg of polystyrene requires a total of equates to the combustion of 130 kg of fossil
most energy is generated by combusting fossil 2.26 kg of fossil oil (1 kg of fossil fuel to gener- fuels per ton of processed grain13.
resources7 (in the US at least), both polymers ate energy and 1.26 kg of fossil fuel to serve as Several fermentation-based PHA process-
also have a latent fossil fuel content. This sug- feedstocks for polymer production; see Table 1 es have been described14–16. Although they
gests that, despite the use of renewable agri- footnote). differ in the choice of microorganism and
cultural feedstocks, fermentative PHA pro- Production of PHAs, on the other hand, is other process characteristics, all share the fol-

542 NATURE BIOTECHNOLOGY VOL 17 JUNE 1999 http://biotech.nature.com


© 1999 Nature America Inc. • http://biotech.nature.com

FEATURE

Table 4. Energy and fossil fuel equivalents (FFEs) required in the production of poly- agitation; cell wall disruption is required to
styrene versus PHA. release the polymer from the microorgan-
ism; between 0.15 and 0.3 kg of biological
Energy and FFE (per kilogram polymer) waste are generated per kilogram of poly-
Item polystyrene PHA mer; and approximately 3.33 kg of glucose
Energy FFEa Energy FFEa are required to produce 1 kg of PHAs (see
Table 1).
Production of raw materials See belowb 1.78 kgb 31,218 kJc 0.80 kg Using an optimistic high-cell-density PHA
Utilities fermentation as a basis for analysis, a 48 h cul-
Steamd 7.0 kg 0.4 kg 2.78 kg 0.14 kg ture would produce an impressive 190 g/L
Electricitye 0.30 kWh 0.08 kg 5.32 kWh 1.45 kg biomass, of which 150 g/L would be PHA
(79% polymer content). Assuming recovery
Total 2.26 kg 2.39 kg
of 100% of the polymer produced in the fer-
aFossil fuels required to produce the energy and raw material in the corresponding energy column, taking mentation, this would require 2.39 kg of fossil
into account the primary fuel usage patterns for each industry. For corn wet milling, energy is generated resources (gas, oil, and coal) to produce 1 kg
from natural gas (37%), coal (48%), and petroleum (10%)11. For each megajoule of energy currently con-
sumed by the corn wet milling industry, 370,000 kJ are generated by combusting 7.84 kg of natural gas,
of PHAs.
etc. Petroleum, coal, and gas have a heat of combustion of 42,000 kJ/kg, 25,788 kJ/kg, and 47,218
kJ/kg, respectively. For other conversions, see Table 3. bFeedstock required to produce 1 kg of poly- The hard facts
styrene from crude oil. The feedstock for direct polymer synthesis is included, as well as a fraction that is
lost in the process and recycled for energy generation. As this type of process does not allow a clear allo-
As the analysis above indicates, the amount
cation of feedstocks, energy numbers include both feedstock and process energy. The analysis does not, of fossil fuel (2.39 kg) required to produce 1
however, include the itemized steam and electricity energy listed below (see also ref. 6). cEnergy (includ- kg of PHAs exceeds that (2.26 kg) required
© 1999 Nature America Inc. • http://biotech.nature.com

ing steam and electrical power) to produce glucose, ammonia, and water. Calculations: 3.33 (yield of to produce an equal amount of polystyrene
PHA on glucose) ´ 8,128 kJ (see Table 2) + 4,028 kJ (energy to produce 0.109 kg of ammonia) + 120 kJ
(energy to provide 26 L of process water) = 31,218 kJ. dThe production of 1 kg of steam requires the com- (see Tables 3 and 4). While the consumption
bustion of 0.058 kg of residual fuel oil during PS production. Fermentation for PHA most likely will use of fossil resources does not differ greatly
natural gas for steam generation and therefore requires only 0.0508 kg of gas to produce the same between the two processes, the emissions
amount of steam. eFor conversion of kWh to FFE, see Table 3.
reveal a discouraging fact: PHA production
requires the combustion of the entire 2.39 kg
lowing features: they can yield very high PHA ing; 2.4 kg of carbon dioxide are emitted per for energy production, whereas polystyrene
concentrations, commonly above 100 g/L; kilogram of polymer produced during the production combusts only 1 kg of the 2.26 kg
biological polymer synthesis is an exothermic fermentation; all processes are aerobic and fossil fuel required for its manufacture, the
process and therefore requires external cool- therefore require considerable aeration and balance being used as a feedstock.
© 1999 Nature America Inc. • http://biotech.nature.com

FEATURE

The energy consumption estimates used in increased biological oxygen demand. Proper that have to be combusted to provide process energy.
9. Smil, V., Nachman, P. & Long, T.V.I. Energy analysis
the analysis above are very conservative and incineration, on the other hand, produces less and agriculture, an application to U.S. corn produc-
far below those of other researchers who have harmful greenhouse gases and, more impor- tion (Westview Press, Inc., Boulder, CO; 1983).
assigned energy requirements to PHA fermen- tantly, allows the partial recovery of energy 10. Pimentel, D. & Pimentel, S. New directions for agri-
culture and agricultural research (ed. Dahlberg, K.A.)
tation processes15. In fact, van Wegen and co- expended during manufacture. (Rowman and Allanheld, Totawa, NJ; 1986).
workers15, who analyzed the fermentation The production of PHAs using corn as a 11. Shapouri, H., Duffield, J.A. & Graboski, M.S.
Estimating the net energy balance of corn ethanol.
process alone and assigned energy values that feedstock with current fermentation technolo- Agricultural Economic Rep. No. 721 (USDA,
were 57% and 467% greater than those used in gy is thus of questionable environmental bene- Washington, DC; 1995).
the present analysis for electricity and steam, fit, even under rather favorable assumptions. 12. Fossil fuels used in U.S. farming are 10% coal, 49%
natural gas, and 40% petroleum.
respectively. If their values were used, the net Although biological processes that use renew- 13. US Department of Energy. Energy Information
effect would be fairly drastic, resulting in an able resources certainly have the potential to Administration of the U.S. Department of Energy,
Manufacturing Consumption of Energy 1991. (Office of
overall fossil fuel consumption of 3.73 kg per conserve fossil resources, this case study Energy, Markets and End Use, Washington DC; 1994).
kilogram of PHAs. demonstrates that such an approach can also 14. Lee, S.-Y. & Choi, J.I. Polymer Degrad. Stability 59,
have the reverse effect. Therefore, future 387–393 (1998).
15. van Wegen, R.J., Ling, Y. & Middelberg, A.P.J. Trans. I
Conclusions assessments of biological processes must not ChemE, Part A 76, 417–426 (1998).
For the particular system studied, the replace- only incorporate the use of raw materials 16. Lee, S-Y. Trends Biotechnol. 14, 431–438 (1996).
17. Reese, K.M. Chem. Eng. News 67, 60 (1989).
ment of conventional polymers with fermen- (which are mostly renewable), but also address 18. Byrom D. 08/09/93 US Patent 5,364,778.
tation-derived PHAs does not appear to be a the indirect consumption of nonrenewable 19. Source: USDA—Economic Research Service.
useful approach if a sustainable production of energy sources required for the process. 20. The census of manufacturing data for energy con-
sumption is based on calendar years, whereas corn
polymers is the desired outcome. Other bene- processing data is based on the harvesting cycle
fits such as the biodegradability and biocom-
© 1999 Nature America Inc. • http://biotech.nature.com

starting with September 1 of a given year. The data


1. Alper, J. Science 283, 1625–1626 (1999). correlated are for the calendar year 1991 and the har-
patibility of PHAs could justify the expense of 2. Pool, R. Science 245, 1187–1189 (1989). vesting cycle starting September 1, 1990 and ending
considerable fossil resources; however, those 3. Williams, S.F. & Peoples, O.P. Chemtech 26, 38–44 August, 31, 1991.
(1996). 21. Hocking, M.B. Handbook of chemical technology and
benefits would have to be quantified and eval- 4. Lee, S-Y. Nat. Biotechnol. 15, 17–18 (1997). pollution control (Academic Press, San Diego; 1993).
uated separately. For example, the usefulness 5. Hocking, M.B. Science 251, 504–505 (1991). 22. Ulrich, G.D. A guide to chemical engineering.
of biodegradability itself has been put into 6. Hocking, M.B. Environ. Management 15, 731–747 Process design and economics. (John Wiley & Sons,
(1991). New York; 1984).
question because the degradation of 7. Energy Information Administration, Department of 23. Atkinson, B. & Mavituna, F. Biochemical engineering
biodegradable materials, such as paper in Energy, http://www.eia.doe.gov/ and biotechnology handbook, 2nd edn. (Stockton
8. While all the carbon dioxide that is emitted during the Press, New York; 1991).
landfills, is not only slow17, but also results in fermentation is indeed of plant origin and therefore 24. Charles, M. & Wilson, J. Bioprocess engineering. (eds
greenhouse gas emissions (methane and car- should not be viewed as a net greenhouse gas contri- Lydersen, B.J., D’Elia, N.A. & Nelson, K.L.) (John
bon dioxide) as well as leachates with bution, this is not the case for the 2.39 kg of fossil fuels Wiley & Sons, New York; 1994).

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