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First published online September 5, 2008
Journal of Experimental Biology 211, 3020-3027 (2008)
Published by The Company of Biologists 2008
doi: 10.1242/jeb.016360
Natural odor ligands for olfactory receptor neurons of the female mosquito Aedes aegypti: use of gas chromatography-linked single sensillum recordings
1 SLU, Department of Plant Protection Biology, 230 53 Alnarp, Sweden
2 Department of Plant Protection, College of Agriculture, Gorgan University of
Agricultural Sciences and Natural Resources, Gorgan, Iran
3 Max Plank Institute for Chemical Ecology, Department of Evolutionary
Neuroethology, DE-07745 Jena, Germany
* Author for correspondence (e-mail: majid.ghaninia{at}vv.slu.se)
Accepted 16 July 2008
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Summary |
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 TOP Summary INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Key words: Aedes aegypti, biologically active volatiles, electrophysiology, olfactory receptor neurons
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INTRODUCTION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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; Monath,
1989). Diseases transmitted to humans by female Aedes
aegypti, dengue and yellow fever, have emerged as a major public health
problem (Gubler, 1989;
Monath, 1989;
Scott et al., 1993). The
mechanisms by which these vectors locate their human hosts, nectar sources and
oviposition sites are primarily olfactory driven
(Takken and Knols, 1999).
Electrophysiological analyses have shown that odor molecules are detected by
olfactory receptor neurons (ORNs) that are mainly housed in antennal trichoid
and grooved peg sensilla (Bentley and Day,
1989; Davis and Bowen,
1994; Davis and Rebert,
1972; McIver,
1982).
Attempts made to unravel the identity of compounds affecting mosquito
behavior (Meijerink et al.,
2000; Qiu et al.,
2004; Qiu et al.,
2006), have provided broad insight into human-emitted volatiles
(Bernier et al., 2000;
Bernier et al., 2002;
Bernier et al., 2003;
Curran et al., 2005). Through
behavioral as well as electrophysiological studies, a handful of mosquito
attractants have been identified from human emanates. We know, for example,
that L-lactic acid, which is detected by specific ORNs housed in
grooved peg sensilla of female Ae. aegypti
(Davis and Sokolove, 1976), in
synergy with carbon dioxide (CO2) elicit a significant attraction
of mosquitoes towards their hosts (Bernier
et al., 2003; Constantini et
al., 1993; Dekker et al.,
2002; Snow, 1970;
Steib et al., 2001). Moreover,
differential attractiveness of human hosts to mosquitoes has been attributed
to the amount of lactic acid present in the host's skin
(Dekker et al., 2002;
Steib et al., 2001). Presence
of CO2 receptor neurons, which reside in maxillary palp sensilla,
was first reported by Kellogg (Kellogg,
1970). Carbon dioxide is exhaled from vertebrates and plays an
important role in the location of hosts by mosquitoes, particularly for
zoophilic species (De Jong and Knols,
1995; De Jong and Knols,
1996; Dekker et al.,
2005; Snow, 1970).
Attraction of females of Ae. aegypti and the African malaria
mosquito, Anopheles gambiae, to incubated human sweat has been shown
to be due mainly to the presence of ammonia, produced through microbial
activity on the skin (Braks and Takken,
1999; Geier et al.,
1999). This compound, which also has a synergistic effect on the
behavioral response to L-lactic acid, is detected by grooved
peg-associated ORNs (Geier et al.,
1999; Meijerink et al.,
2001). In addition, short- to medium-chain fatty acids and
1-octen-3-ol (octenol) emanating from human hosts have also been shown to
elicit both electrophysiological and behavioral responses in female Ae.
aegypti (Bosch et al.,
2000; Bowen, 1992;
Kline et al., 1990;
Knols and Meijerink, 1997;
Meijerink and van Loon, 1999).
Moreover, there is ample evidence suggesting that additional compounds are
exploited by mosquitoes to locate their hosts
(Bosch et al., 2000;
Geier et al., 1999;
Qiu et al., 2006). Chemical
analysis of human skin headspace collections has revealed at least 277
compounds (Bernier et al.,
2000). Which of these compounds are detected by mosquito ORNs and
what role these play in regulating behavioral attraction towards human hosts
is, however, largely unknown.
Plants also constitute relevant odor sources for mosquitoes. Almost all
mosquitoes require sugar resources, which are derived from flowers and
extrafloral nectaries of their host plants
(Takken and Knols, 1999).
Orientation and attraction of mosquitoes to their host plant has been shown to
be mediated by volatiles given off from the plant
(Takken and Knols, 1999). A
few host plant-related compounds have been shown to be detected by ORNs of
mosquitoes (Bowen, 1992;
Davis, 1977). Some plant
species are, however, repellent to mosquitoes
(Curtis et al., 1991).
Olfactory receptor neurons responsible for the detection of the active
component(s) of these plants have not been reported.
In the present study, we have exploited the specificity and sensitivity of
gas chromatography-linked single sensillum recordings (GC–SSRs) from
female Ae. aegypti in order to identify novel biologically active
volatile compounds. Apart from the previously characterized trichoid sensilla
(Ghaninia et al., 2007) we
performed GC–SSRs from intermediate sensilla in order to expand our
knowledge concerning olfactory coding in this species. In order to identify
compounds potentially used by Ae. aegypti for orientation towards
their human host, we collected volatile samples from feet, trunk (chest and
urogenital) regions, armpits and urine. We also collected volatiles from
catnip, Nepeta faassenii (Lamiaceae). Species within the genus
Nepeta contain volatile compounds that act as strong attraction
inhibitors to mosquitoes (Amer and
Mehlhorn, 2006a; Amer and
Mehlhorn, 2006b).
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MATERIALS AND METHODS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Headspace samples
Headspace samples were collected by placing odor sources in 3 l polyacetate
oven bags, through which charcoal-purified air was circulated by means of an
electric pump (KNF Neuberger, Stockholm, Sweden). Volatiles were trapped on
filters with two compartments, containing 150+75 mg Porapak Q (Supelco)
situated at the exhaust of the bag. Volatile collections lasted between 24 and
48 h. Extracts were prepared by rinsing filters with 800 µl of distilled
hexane and concentrated to approximately one-third of the volume before
use.
Armpit odor sampling
The method that we used for armpit sampling has been provided by Curran et
al. (Curran et al., 2005). Ten
volunteers (eight males and two females, 29–39 years old) were given two
double-layer sterile gauze pads (7x10 cm) to attach under their armpits
for two consecutive days. The volunteers were also instructed to follow their
daily life but not to use deodorant, perfumes and lotions and not to take a
shower during this period. After 48 h, the pads were pooled and subjected to
odor collection.
Foot and trunk odor sampling
Fifteen male and five female volunteers aged 25–45 years were subject
to foot odor sampling. All volunteers were given fresh socks to wear for 48 h
as they do in their daily life. Some of the volunteers performed physical
exercise. To collect volatiles from trunk regions three males and one female
volunteer gave us their undergarments. Headspace collections and extractions
of the volatiles from feet (through the pooled socks) and trunk regions
(through the pooled undergarments) were performed as described above.
Urine odor sampling
Urine from two male volunteers collected in a glass bowl was put into
polyacetate food bag for headspace collection.
Plant volatiles sampling
Whole, potted, Nepeta faassenii plants were placed inside the
collection bags for plant odor collection.
Mud volatiles sampling
Mud samples were collected from two small standing water lakes located in
the vicinity of the institute, in a plastic tray (20x18x7 cm). The
tray was then conveyed to the institute and placed in collection bags.
Electrophysiology
Mosquito preparation
A female mosquito was cooled by placing it in a –5°C freezer for
1-2 min and then glued to a piece of double-sided sticky tape on a
microscope slide (76x26 mm). The animal was secured by covering half of
the thorax and the abdomen by tape. The antenna was lifted and placed on a
small coverslip (18x18 mm) bearing a piece of double-sided sticky tape.
The antenna of the mounted animal was viewed through an Olympus light
microscope (BX51W1), which allowed for a highly magnified (750x) view of
the sensilla on all antennal segments.
Single-sensillum recordings (SSR) and gas chromatography (GC)-linked SSRs
Single sensillum recordings and GC–SSRs were performed according to
standard protocols described by Stensmyr et al.
(Stensmyr et al., 2003) and
Ghaninia et al. (Ghaninia et al.,
2007). Briefly, a sharpened tungsten microelectrode with a 1
µm tip diameter was inserted into the eye. A second tungsten microelectrode
was positioned at the base of a sensillum until electrical contact with the
sensillum was established (Fig.
1). Action potentials of the ORNs housed in the sensillum were
amplified through a USB-IDAC interface amplifier (Syntech, Kirchzarten,
Germany), displayed on a computer screen and recorded for further
investigations. SSRs were performed on previously characterized functional
classes of trichoid sensilla (Ghaninia et
al., 2007), as well as intermediate sensilla
(Fig. 2). In order to identify
the functional type of trichoid sensilla, we delivered a set of diagnostic
compounds (see Ghaninia et al.,
2007). After characterization, the activity of each biological
extract was determined by stimulating the sensillum with 10 µl of each
extract, pipetted on a piece of filter paper (5x20 mm) placed inside a
Pasteur pipette. When an extract elicited responses from the ORNs, 2 µl of
the extract was subsequently injected into a GC linked to the SSR recording
setup via a heated transfer line (see below; Figs
1 and
3). Occasionally, contacts were
lost before running the GC–SSR owing to inevitable environmental
vibrations or animal muscle contractions, which may cause damage to the
receptor neurons. Successful electrophysiological data were recorded and
processed by means of Autospike 3 (Syntech). Spikes from neurons present in
single sensilla were differentiated based on spike amplitude, where the larger
amplitudes were denoted as A and the smaller amplitudes as B
(Fig. 3A,B).
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Chemical identification
Identification of active compounds in the extracts was performed by means
of coupled gas chromatography–mass spectrometry (GC–MS). Each
extract (2 µl) was injected into a 6890N gas chromatograph (Agilent
Technologies) coupled to a 5975 mass spectrometer (Agilent Technologies).
Compounds were separated on a polar capillary column DB-WAX (30 mx0.25
mm inner diameter coated with chromatographic film with 0.25 µm film
thickness). Carrier gas was helium (speed 36 cm s–1). The
oven temperature was held at 40°C for 2 min and then increased at 10°C
min–1 to a final temperature of 230°C, which was held for
10 min.
The identity of active compounds was determined by comparison with references from mass spectral libraries (NIST05, Agilent Technologies). Final confirmation of identity was achieved by co-injection with synthetic reference compounds when these could be obtained.
Dose–response relationships
For verification of the physiological activity of chemicals identified
through GC–MS, dose–response experiments were performed on the
responding cells with synthetic reference chemicals when these could be
obtained. The net response to a stimulus was quantified as the number of
spikes 0.5 s after stimulation minus 0.5 s before stimulation. The outcome was
then multiplied by two. Concentration of each synthetic compound ranged from
0.001 to 10% (v/v), dissolved in paraffin oil. Delivery of the compounds and
analysis of the responses are described by Ghaninia et al.
(Ghaninia et al., 2007).
Synthetic compounds
Compounds used for physiological characterization of sensilla were obtained
from commercial suppliers (Ghaninia et
al., 2007). Synthetic references for confirmation of chemical
identity and dose–response experiments in this study were obtained from
SAFC (heptanal, +92%), Fluka (octanal, 
98%; nonanal, 95%) and Sigma
(decanal, 99%)
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RESULTS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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)
(Table 1). A schematic drawing
of all trichoid sensillum types together with the approximate distribution of
their various functional types are shown in
Fig. 2
(Ghaninia et al., 2007). Most
neurons had spontaneous activity ranging from 20 to 30 Hz. There appeared to
be no consistent differences in spontaneous activity between sensillum types;
we would rather attribute differences between individual sensilla to an effect
of electrode penetration discussed by Meijerink et al.
(Meijerink et al., 1999). Of
the sensilla encountered in the present study, we managed to perform 25
successful GC–SSR runs on the nine previously defined trichoid sensillum
types (Ghaninia et al., 2007)
as well as on three novel types of intermediate sensilla, which we term i-1,
i-2 and i-3 (Table 1).
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Based on the number of FID peaks, all extracts contained roughly between 30 and 70 compounds (data not shown). Only four extract types (feet, trunk, armpit and Nepeta) elicited a response from antennal ORNs (Table 1), to a total of 12 FID peaks (components) (Table 2). Examples of chromatograms produced from different extract types, along with ORN responses corresponding to the peaks, are shown in Fig. 4. Overall, eight responding compounds, i.e. heptanal, octanal, nonanal, decanal, dodecanal, 2,6-dimethyl-2,6-octadien, geranylacetone (6,10-dimethyl-5,9-undecadien-2-one) and nepetalactone, were identified through GC–MS analyses (Table 2). Four of these compounds were verified by commercially available synthetic standards and their biological activity was confirmed by dose–response experiments (Fig. 5). The mass spectra of four physiologically active compounds could not be matched to any reference mass spectrum and are listed as `unknown' (Table 2). Neither urine nor mud headspace extracts elicited a response in any of the ORN types tested (Table 1). These extracts contained the same complexity of peaks as seen in, for example, feet and trunk extracts (data not shown).
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Overall, ORNs were narrowly tuned to one or a few components present in the extracts. Of the short sharp trichoid (sst) sensilla, only sst-4 responded to one of the extracts tested (trunk extract). However, damage to this sensillum during the recording process did not allow us to run a GC–SSR experiment, and this type was not found again during the experiments (Table 1). The `A' neuron of the short blunt trichoid sensillum type I (sbtI1-A) responded only to the Nepeta extract, with the active compound identified as nepetalactone (Table 2). The sbtII-2A cell detected the highest number of extract components (six in total): heptanal, octanal, nonanal, decanal, 2,6-dimethyl-2,6-octadien and geranylacetone (Table 2). None of the extracts elicited a response in long sharp (ls) trichoid sensilla (Table 1).
Based on GC–SSR analysis, we were able to define three novel
functional classes of intermediate sensilla. These sensilla resemble the four
distinct morphological types of the sensilla trichodea but vary in length
(Davis and Rebert, 1972)
(M.G., unpublished) and displayed unique responses to the tested extracts
(Table 1). One of the
intermediate sensillum types, i-1, responded to trunk volatiles, decanal and
`unknown 2' (Table 2). Five
components, found in extracts of feet, trunk and Nepeta, activated
the i-2A cell. We were able to identify two of these compounds as dodecanal
and geranylacetone (Table 2).
We observed a response of the i-2A neuron to the armpit extract but were
unable to perform a GC–SSR run (Table
1). The A-neuron of the third intermediate sensillum type, i-3A,
responded to a single compound in the trunk headspace extract
(Table 1), later identified as
geranylacetone (Table 2).
Dose–response experiments
In order to evaluate the sensitivity of the identified ORNs to the novel
ligands, we obtained dose–response relationships for two of the
functional classes of sensilla, sbtII-2 and i-1
(Fig. 5A,B). This was conducted
by exposing the sensilla to different concentrations of the synthetic
compounds (Table 2,
Fig. 5C-L; see also Materials
and Methods). The most potent stimulus, nonanal, elicited a significant
response at 0.01% (Fig. 5A).
The sensitivity threshold for nonanal was close to 0.001%, whereas the
thresholds for octanal, heptanal and decanal were 10- or 100-fold higher. The
responses to nonanal and octanal peaked at concentrations of 0.1% and 1%,
respectively, and thereafter a reduction or no change in the response to
higher concentrations was observed (Fig.
5A). The `A' neuron of the intermediate sensillum, i-1A, exhibited
a dose-dependent response to decanal with a response threshold of 0.1%
(Fig. 5B).
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DISCUSSION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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;
Qiu, 2005).
Through systematic GC–SSRs from physiologically characterized
sensilla, we have been able to identify eight natural odor ligands from
different headspace extracts that are detected by the ORNs of female Ae.
aegypti. All the compounds identified in this study, except for
2,6-dimethyl-2,6-octadien, which, to our knowledge, represents a novel
component of human skin, have previously been reported to be present in human
skin emanations or in Nepeta species volatiles
(Bernier et al., 2000;
Bernier et al., 2002;
Curran et al., 2005;
McElvain et al., 1941). An
interesting observation is that heptanal, octanal, nonanal and decanal, which
are present in either fresh and/or incubated human sweat
(Meijerink et al., 2000), are
detected by ORNs of Ae. aegypti (present study) but were not found to
elicit a response in female An. gambiae antennal ORNs using the EAG
technique (Meijerink et al.,
2000). This observation may be due to low resolution of the latter
technique and/or it might be linked to the partial divergence of the Ae.
aegypti and An. gambiae olfactory receptor repertoire
(Bohbot et al., 2007). Future
studies, including heterologous expression and behavioral studies will have to
be designed to address this issue. Although some weak electrophysiological
responses of the maxillary palp-associated ORNs to the above-mentioned
aldehydes were reported in An. gambiae and Culex
quinquefasciatus (Lu et al.,
2007; Syed and Leal,
2007), until recently almost nothing was known about the
behavioral importance of these compounds in mosquito life. Recently,
GC–EAD studies of human-derived headspace have revealed some compounds
identical to those found in the present study. The compounds included octanal,
nonanal, decanal, dodecanal and geranylacetone, to which mosquitoes responded
behaviorally (Logan et al.,
2008).
The origin of human-specific volatiles emanating from different body
regions has been attributed to the aggregation of diverse communities of
microbiota (Braks et al.,
1999). It has therefore been suggested that differences in
microbiota on the human skin play an important role in generating individual
body odors, driving the attraction of mosquitoes to different host individuals
and even different body regions (Braks et
al., 1999). Quantitative as well as qualitative differences of
specific body odors have been suggested to underlie this differential
attraction (Bernier et al.,
2002; Penn et al.,
2006). In the present study, GC–SSRs revealed that Ae.
aegypti ORNs responded to octanal, nonanal and decanal. These compounds
have previously been reported to be present in differing ratio patterns
between individuals, indicating qualitative similarities among individuals
with quantitative differences (Bernier et
al., 2002; Curran et al.,
2005). By contrast, 2,6-dimethyl-2,6 octadien and
6,10-dimethyl-5,9-undecadien-2-one were found at physiologically active levels
exclusively in trunk headspace extracts, indicating a qualitative difference
between body regions. The latter compound has previously been reported to be
present in most but not all human individuals
(Bernier et al., 2005). In
conclusion, the peripheral olfactory system of female Ae. aegypti
contains ORNs capable of detecting compounds that could be used to
differentiate between individual hosts and even body regions. Behavioral
studies have to be conducted to verify the role of these compounds in the
complete volatile blend that mediates host attraction.
In addition to responses to human volatiles, we observed responses to
nepetalactone in sbtI1 sensilla. Nepetalactone is the primary component of
catnip oil, the vapors of which have been shown to be repellent to a diverse
number of insect species, including mosquitoes
(Amer and Mehlhorn, 2006a;
Eisner, 1964;
Peterson and Coats, 2001;
Peterson et al., 2002). In
behavioral tests, nepetalactone acts as a `spatial repellent', inhibiting the
landing rate of Ae. aegypti and other mosquito species more than the
commonly used synthetic mosquito repellent DEET
(Bernier et al., 2005;
Hui-Ling et al., 2006;
Peterson and Coats, 2001).
Overall, very few ORNs associated with trichoid sensilla responded to the
extracts tested. We assume that other sensillum types, i.e. grooved pegs as
well as intermediate sensilla (as our study shows), might be involved in the
detection of the current extract-associated components. Problems with odor
collection/extraction of some human related compounds have also been reported
(Bernier et al., 2000;
Cork and Park, 1996).
To this date, laboratory and field studies indicate that the use of
CO2 is one of the few environmentally safe procedures to suppress
mosquito densities (Knols et al.,
1994; Knols et al.,
1998). Although CO2 plays an important role in
attracting mosquitoes in the field, this compound is non-specific.
CO2-baited traps predominantly catch zoophilic mosquitoes whereas
highly anthropophilic mosquitoes, which seem to require additional
attractants, show limited attraction to the traps
(Constantini et al., 1993;
Knols et al., 1998;
Mboera et al., 2000).
Furthermore, application of CO2 in the field is costly; it needs to
be transported into the field in pressurized gas cylinders or as dry ice
(Bernier et al., 2003;
Curtis, 1996;
Knols et al., 1994;
Knols et al., 1998;
Mboera et al., 2000). By
contrast, the use of human-associated kairomones is considered as a good
alternative method for collecting, monitoring or controlling host-seeking
mosquitoes, as these in a series of behavioral tests in the laboratory and
field have shown to elicit high levels of attraction without the presence of
CO2 (Bernier et al.,
2003; Edman, 1979;
Eiras and Jepson, 1991;
Eiras and Jepson, 1994;
Gillies and Wilkes, 1974;
Silva et al., 2005). The use
of GC–SSRs and other analytical methods will be valuable for selecting
additional kairomone compounds to optimize an attractive bait.
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Acknowledgments |
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References |
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