Formation of lipid reserves in fat body and eggs of the yellow fever mosquito, Aedes aegypti

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Abstract

We examined the accumulation of lipids in adult females of the mosquito, Aedes aegypti. Females emerged with about 100 μg lipid in the fat body. With access to sugar water lipids increased over seven days to 300 μg. After a blood meal on day five, sugar-fed females accumulated 120–140 μg of lipids in their ovaries within 2 days. At the same time the lipid content of the fat body decreased by 100 μg, indicating transfer of lipids from fat body to oocytes. Experiments in which fat body lipids were prelabelled support this conclusion. Label was transferred to oocytes: in mature oocytes the specific radioactivity of lipids was 80% of the specific radioactivity of prelabeled fat body lipids. Components of blood meals are also used to synthesize oocyte lipids. Fat bodies of females starved for four days had only 27 μg of lipids left. When these females were given a blood meal, they matured oocytes, although the number of ooyctes was reduced and ovaries contained only half the amount of lipids found in ovaries of females which had first fed on sugar water. Fat body lipids of these females had only slightly increased to 36 μg. This demonstrates that female Ae. aegypti use sugar to synthesize lipids, but they can also use components of blood for this purpose.

Introduction

Mosquitoes, like other insects, can store large amounts of lipids in their fat body, which is the major energy storage site in insects. These lipid reserves are either carried over from the larvae or they are formed from food ingested by adults. Females of most mosquitoes feed on sugar water as well as on blood (Foster, 1995). It was shown that females of Aedes sollicitans form large amounts of lipids after ingestion of sugar water (Van Handel, 1965). Recently it has been questioned whether free living Ae. aegypti feed on sugar water (Foster, 1995). We did not examine free living Ae. aegypti, but in the laboratory females of Ae. aegypti feed readily on sugar water and, as our results show, they form large amounts of lipids from sugar.

Yolk-rich eggs contain, in addition to protein, large amounts of lipids. In Manduca sexta 40% of the dry weight of eggs is lipids (Kawooya and Law, 1988). Oocytes of the yellow fever mosquito, Ae. aegypti, were found to contain 35% lipids (Troy et al., 1975), although the percentage of lipids varies according to the size and nutritional status of the female (Briegel, 1990). An important role of these egg lipids is to supply energy, which is needed by the developing embryo. In Culex quinquefasciatus it was shown that about 90% of this energy is derived from lipids (Van Handel, 1993). This clearly indicates the importance of lipids for reproduction of mosquitoes.

The large amounts of lipids found in the oocytes, could be synthesized in the ovaries or in some other tissue, most likely the fat body, and then transported to the oocytes. The capacity of oocytes and other tissues to synthesize lipids in vitro has been examined previously (Ziegler, 1997). Only very minor synthesis of fatty acids was observed to occur in oocytes. Moreover, fatty acids synthesized by the ovaries are mostly incorporated into phospholipids, while the majority of lipids stored in this tissue are triacylglycerols (TAG). The fat body synthesizes fatty acids in vitro, most of which are incorporated into TAG. The gut was found to synthesize no fatty acids (Ziegler, 1997). This corresponds well with results obtained in M. sexta (Kawooya and Law, 1988).

Ovaries of sugar fed Ae. aegypti contain only traces of lipids. The accumulation of proteins and lipids in the oocytes starts only after a blood meal and the lipid complement is deposited within 48 h after the blood meal (Troy et al., 1975). The lipids stored in oocytes could therefore be derived from lipids synthesized by fat body from sugar taken up before the blood meal is ingested, or the lipids could be derived from components of the blood meal.

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Materials and methods

Aedes aegypti (NIH–Rockefeller strain) were reared at 28±0.5°C, 80% relative humidity and a photoperiod of 16:8 h, using standard techniques (Baker et al., 1983). Larvae were raised in batches of 2000 in a 5 inch deep pan measuring 56×30 in., containing about 1.5 in. of water. Adult mosquitoes had free access to 10% sugar water on a cotton ball. Depending on the experiment, 4, 5 or 6 days after emergence, females had one blood meal on an anesthetized rabbit. We measured the lipid content of fat

Results

Because the fat body is the major site of lipid synthesis and storage, we followed the lipid content of the fat body of sugar-feeding females from emergence to day eight. At emergence, the fat body of females contained about 100 μg of lipids. On the first day of adult life a small decrease in lipids was observed, but then the amount of lipids increased, mostly between day two and five. After day five the increase leveled off and the maximum lipid content was reached by about day seven at 300 μg

Discussion

Sugar is the basic food for adult mosquitoes (Foster, 1995), which they can convert to lipids (Van Handel, 1965). The occurrence of sugar feeding in female Ae. aegypti, however, is disputed (Foster, 1995). It was even concluded “that it was advantageous, from the perspective of accumulating energy reserves, for Ae. aegypti to feed on human blood early in adult life, that is, during the second or perhaps third day after emergence” (Naksathit et al., 1999a). These authors followed the

Acknowledgements

This work was supported by grants from NIH GM 29238 and from Deutsche Forschungsgemeinschaft Zi 135/10-1. M.M.I. was supported by grant No. 71195-521304 from HHMI to the UA Undergraduate Biology Research Program.

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Present address: Department of Pharmacology and Toxicology, The University of Arizona, Tucson, AZ, USA.

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