NATURE BIOTECHNOLOGY VOLUME 30 NUMBER 1 JANUARY 2012 35
that participates in critical host physiological
processes, thereby minimizing nontarget
effects.
Insect diuretic hormones participate in
the regulation of water balance, and MSDH
belongs to the corticotropin-releasing factor–
related family of peptides. Synthetic MSDH
has been shown to stimulate fluid excretion
in vivo, resulting in pronounced loss of
fluid through the gut and the epidermis,
decreased feeding and ultimately insect
death
8–10
. TMOFs are unblocked deca-
and hexa-peptides that terminate trypsin
biosynthesis in the insect gut and are found
in the ovaries of insects that include both
mosquitoes and flies. Aea-TMOF circulates
in the hemolymph, binds to gut receptors
on the hemolymph side of the gut and
inhibits trypsin biosynthesis by exerting a
translational control on trypsin mRNA
11
.
Because TMOF resists proteolysis in the gut
and easily traverses the gut epithelial cells
into the hemolymph in adults and larvae,
it was fed to different species of mosquito
larvae in which it caused inhibition of food
digestion and anorexia, ultimately leading to
starvation and death
12
. TMOF is currently
under development as an insecticide
and appears to be very specific against
mosquitoes with minimal nontarget effects
13
.
Indeed, TMOFs from different insects have
different peptide sequences (e.g., the Aea-
TMOF sequence is YDPAPPPPPP, whereas
the gray flesh fly, Sarcophaga bullata, Sb-
TMOF sequence is NPTNLH
14
).
MSDH-Gly (42 amino acids) and the
A. aegypti Aea-TMOF peptides were
expressed in B. bassiana by transformation of
expression vectors containing a constitutive
B. bassiana-derived gpd promoter and the
nucleotide sequence corresponding to the
insecticides has resulted in substantial
damage to ecosystems and the emergence
of insecticide-resistant agricultural pests.
Mosquitoes are vectors of many human
and animal infectious diseases that cause
death and economic hardship. World
Health Organization (WHO; Geneva)
recommendations suggest the use of different
control strategies as part of integrated
vector management control to prevent
the emergence of insecticide-resistant
mosquitoes. Effective strategies, however, for
long-term reduction of mosquito populations
remain elusive
2
. Entomopathogenic fungi
are virulent to a wide range of Lepidoptera
as well as mosquitoes and have been
considered as possible candidates for
reducing disease transmission of vector-
borne infectious agents
3,4
. Methods have
been developed for delivery of these agents
in agricultural settings as well as to adult
and larval mosquitoes, and the fungi appear
to be equally (or more) effective against
insecticide-resistant strains as compared
with their insecticide-susceptible parental
strains
5–7
.
To test whether host molecules can
be used to increase the virulence of
entomopathogenic fungi, we engineered two
insect peptides—Manduca sexta diuretic
hormone (MSDH) and A. aegypti trypsin-
modulating oostatic factor (Aea-TMOF)—in
B. bassiana, which expresses and secretes
these hormones as it infects its host. Our
idea was that the exogenously produced host
peptide hormone would disrupt the normal
endocrine or neurological balance of the host,
making it more susceptible to the invading
fungus. As candidates, we chose a potential
broad host range target (MSDH) as well as
a more host-specific peptide (TMOF) target
Exploiting host molecules to augment
mycoinsecticide virulence
To the Editor:
A pressing need exists for additional
tools in insect control, particularly as
few new chemical pesticides are under
development. Entomopathogenic fungi, such
as Metarhizium anisopliae and Beauveria
bassiana, both US Environmental Protection
Agency (EPA)-approved biological control
agents, offer an environmentally friendly
alternative to chemical insecticides. One
limitation to the use of entomopathogenic
fungi is the relatively long time (6–12
days) it takes for the fungus to kill target
insects. Expression of a scorpion toxin in
M. anisopliae increases fungal toxicity about
ninefold toward the yellow fever mosquito,
Aedes aegypti
1
; however, expression of
nonspecies-specific toxins to control
mosquitoes may promote the development
of toxin resistance. Ideally, a strain with
enhanced virulence toward target insects
with minimal nontarget effects, coupled to
a decreased likelihood of the development
of resistance to the agent is most desired.
To meet this objective, we report a novel
approach to insect control, in which
expression of host molecules in an insect
pathogen is exploited for augmentation of
virulence.
The major advantages of such a strategy
are the following: first, the increase in
virulence can be tailored to be host specific
depending upon the host molecule (peptide)
chosen; and second, the development of
resistance can be minimized as the host
peptide hormones regulate developmental
processes that are species and tissue
specific. Contrary to current approaches
in insect control, mutations that arise and
could compensate for the fungal-expressed
product during infection, also would lead
to developmental defects—a fitness cost
far greater than developing resistance to a
pesticide. Thus, unlike methods that use
insecticidal compounds, the development
of resistance using our approach faces an
additional burden. In theory, multiple host
molecules can be expressed in the same fungal
strain to further augment the specificity and
virulence of mycoinsecticides to produce the
next generation of more effective and safer
insect biological control agents.
Lepidopteran species cause billions of
dollars worth of crop losses worldwide and
are the most destructive pests in agriculture.
Overuse and reliance on chemical
Table 1 Calculated LD
50
and LT
50
of wild-type, MSDH- and TMOF-expressing
B. bassiana strains against G. mellonella and A. aegypti
Strain Host LD
50
(conidia/ml) LT
50
(h)
Wild-type B. bassiana G. mellonella 2.4 ± 0.3 × 10
7a
134.7 ± 5.5
b
Bb::spMSDH G. mellonella 0.3 ± 0.10 × 10
7a
86.2 ± 3.8
b
Wild-type B. bassiana A. aegypti (adult) 5.0 ± 0.6 × 10
8c
163.2 ± 12.0
d
Bb::spAeaTMOF A. aegypti (adult) 6.25 ± 0.5 × 10
7c
123.2 ± 9.2
d
Wild-type B. bassiana A. aegypti (larvae) 1 × 10
8e
156 ± 6.6
f
Bb::spAeaTMOF A. aegypti (larvae) 1 × 10
8e
100.8 ± 5.0
f
a
LD
50
calculated from 96-h time point.
b
Bioassay performed using spore concentration of 1 × 10
7
conidia/ml.
c
LD
50
calculated from 120-h time point.
d
Bioassay performed using 0.25 μl of a 1 × 10
8
conidia/ml spore solution applied to
mosquito abdomen.
e
Accurate LD
50
could not be determined in this case.
f
Bioassay performed using spore concentration
of 1 × 10
8
conidia/ml.
CORRESPONDENCE
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