Growth Dynamics of Artemisia annua
Hairy Roots in Three Culture Systems
Yoo Jeong Kim,
1
Pamela J. Weathers,
2
Barbara E. Wyslouzil
1
1
Department of Chemical Engineering, Worcester Polytechnic Institute, 100
Institute Road, Worcester, Massachusetts 01609; telephone:
508-831-5493; fax: 508-831-5853; e-mail: barbaraw@wpi.edu
2
Department of Biology and Biotechnology, Worcester Polytechnic
Institute, 100 Institute Road, Worcester, Massachusetts 01609
Received 26 June 2002; accepted 3 February 2003
DOI: 10.1002/bit.10685
Abstract: The transient growth of Artemisia annua hairy
roots was compared for cultures grown in shake flasks
and in bubble column and mist reactors. Instantaneous
growth rates were obtained by numerically differentiat-
ing the transient biomass measurements. Specific sugar
consumption rates showed good agreement with litera-
ture values. From the growth rate and sugar consump-
tion rate, the specific yield and maintenance coefficient
for sugar were determined for all three culture systems.
These values were statistically indistinguishable for
roots grown in shake flasks and bubble columns. In con-
trast, the values for roots grown in bubble columns and
mist reactors were statistically different, suggesting that
sugar utilization by roots grown in these two systems
may be different. By measuring respiration rates in the
bubble column reactor we also determined the actual
biomass yield and maintenance coefficient for O
2
and
CO
2
. Together with an elemental analysis of the roots,
this allowed us to obtain a reasonable carbon balance.
© 2003 Wiley Periodicals, Inc. Biotechnol Bioeng 83: 428–443,
2003.
INTRODUCTION
Bioreactor design remains a key issue that must be ad-
dressed before secondary metabolite production from hairy
roots can be commercially successful. Developing a deeper
understanding of how transformed roots respond to different
reactor environments is particularly important, and the goal
of our research is to quantitatively assess the relative effec-
tiveness of liquid- and gas-phase reactors for culturing these
plant tissues. In an earlier study (Kim et al., 2001), we found
that the level of artemisinin contained in Artemisia annua
hairy roots was significantly higher in the mist reactor than
in the bubble column, and that the roots grown in shake
flasks contained a negligible amount of artemisinin. On the
other hand, a side-by-side comparative study of the overall
biomass productivity showed that both the effective growth
rate and a 2-week average growth rate were almost always
higher in the bubble column than in the mist reactor (Kim et
al., 2002).
In this paper, we compare the transient growth of A.
annua hairy roots in different reactor environments and de-
termine the nutrient utilization rates. Nutrient utilization
rates for hairy root cultures are usually reported as the ap-
parent biomass yield—the ratio of the amount of nutrient
consumed to the increase in biomass (Bhadra and Shanks,
1997; Kwok and Doran, 1995). The apparent yield can be
further subdivided into the actual yield, a conversion effi-
ciency of the nutrient consumed for biomass gain, and the
maintenance coefficient, the nutrient required to maintain
viability of existing biomass (Schnapp et al., 1991). These
values can provide deeper insight into the bioconversion
process and may clarify the advantages that one reactor
design may have over another. Obtaining actual yield and
maintenance coefficients requires following transient bio-
mass closely, a task that is more difficult for hairy root
cultures than cell suspension cultures. Thus, there is little
data of this type available in the literature.
As in our previous work, we chose a bubble column and
a nutrient mist reactor as representative liquid- and gas-
phase reactors, respectively. We cultured the YUT16 hairy
root clone of A. annua in these two reactors as well as in
shake flasks. We first compared the biomass productivity
and the changes in the major nutrients observed in the re-
actors directly to those observed in shake flask experiments
as a function of time. We then estimated transient biomass
in the reactors during culture, using correlations based on
shake flask experiments, and determined the instantaneous
specific growth rates. The specific growth rates were related
to the specific sugar consumption rates to determine the
actual biomass yield and the maintenance coefficients for
sugar as a function of the culture environment. For the
bubble column reactors, we also measured the specific res-
piration rate, related this to the specific growth rate, and
calculated the actual biomass yield and the maintenance
coefficient for oxygen and carbon dioxide. Finally, using
both actual yields and maintenance coefficients for sugar
and oxygen from the bubble column reactors, we performed
a carbon balance to determine the reliability of our results.
Correspondence to: Barbara E. Wyslouzil, Department of Chemical En-
gineering, 100 Institute Road, Worcester, MA 01609.
Contract grant sponsors: NSF; NIH
Contract grant numbers: BES-9414858; R21AI39170-01
© 2003 Wiley Periodicals, Inc.