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Role of Lipids in Energy Metabolism
Abstract
Most reviews of lipid metabolism in insects have covered all classes of lipid compounds. Since lipids are generally defined as substances poorly soluble in water but soluble in organic solvents, the authors had to deal with compounds with divergent physiological functions, e.g., phospholipids and pheromones. The subject of this chapter limits the lipoidal substances to be discussed to those that provide a direct source of metabolic energy, though we recognize that other important lipid classes, for example those contributing to (sub)cellular components, are also essential for metabolism.
... Lipids and glycogen are important energy resources used for processes such as flight, vitellogenesis and immune responses (Steele, 1981). Glycogen stores are released from within cells and provide a source of energy for immediate flight, whereas ingested carbohydrates are converted to lipids that are directly involved in oogenesis, moulting and sustained flight (Beenakkers et al., 1981). Resource-based trade-offs have been previously observed in insecticide-resistant mosquito populations, with the over-production of detoxifying enzymes requiring an extensive investment of resources. ...
The recent scale-up of insecticide use has led to the rapid spread of insecticide resistance (IR) in mosquito populations across the world. Previous work has suggested that IR mechanisms could influence mosquito life-history traits, leading to alterations in fitness and key physiological functions. This study investigates to what extent mosquito fitness may be affected in a colony of Aedes aegypti after selection with temephos, permethrin or malathion insecticides. We measured immature development, sex ratio, adult longevity, energetic reserves under different rearing conditions and time points, ingested bloodmeal volume, mosquito size, male and female reproductive fitness and flight capability in the unexposed offspring of the three selected strains and unselected strain. We found that insecticide selection does have an impact on mosquito fitness traits in both male and female mosquitoes, with our temephos-exposed strain showing the highest immature development rates, improved adult survival, larger females under crowded rearing and increased sperm number in males. In contrast, this strain showed the poorest reproductive success, demonstrating that insecticide selection leads to trade-offs in life-history traits, which have the potential to either enhance or limit disease transmission potential.
... Decreasing lipid accumulation may then result in an inhibition of Vg protein synthesis leading to a reduction of fecundity in insects. In addition, lipids are an important component of insect oocytes, not only accounting for a significant proportion of oocyte dry weight (30-40%; Kawooya andLaw 1988, Hans 1990) but also providing energy to the embryos (Beenakkers et al. 1981). It can be concluded from the above that lipids do play an important role in insect reproduction. ...
The gut microbiota of insects usually plays an important role in the development and reproduction of their hosts. The fecundity of Henosepilachna vigintioctopunctata (Fabricius) varies greatly when they develop on different host plants. Whether and how the gut microbiota regulates the fecundity of H. vigintioctopunctata was unknown. To address this question, we used 16S rRNA sequencing to analyze the gut microbiomes of H. vigintioctopunctata adults fed on two host plant species (Solanum nigrum and Solanum melongena) and one artificial diet. The development of the ovaries and testes was also examined. Our results revealed that the diversity and abundance of gut microorganisms varied significantly in insects reared on different diets. The gut microbiota of H. vigintioctopunctata raised on the two host plants was similar, with Proteobacteria being the dominant phylum in both groups, whereas Firmicutes was the dominant phylum in the group reared on the artificial diet. The predominant microbiota in the S. nigrum group were Acinetobacter soli and Acinetobacter ursingii (Acinetobacter, Moraxellaceae); Moraxella osloensis (Enhydrobacter, Moraxellaceae); and Empedobacter brevis (Empedobacter, Weeksellaceae). The microbiota in this group are associated with high lipid metabolism. In addition, the beetles' ovaries and testes were more highly developed in the S. nigrum group than in the other two groups. These findings provide valuable information for elucidating the complex roles the gut microbiota play in the fecundity of H. vigintioctopunctata, and may also contribute to developing future novel control strategies involving this economically important pest.
... Shortdistance-travel insects use carbohydrates as their main energy source [26]. The preferred energy source of longdistance-travel insects is carbohydrates, and these insects then change their energy source from carbohydrates to lipids [28]. In most insects, carbohydrates are used as the main energy source because carbohydrates are hydrophilic substances and move faster than lipids into insect bodies. ...
Objective
Insects are the most evolutionarily successful groups of organisms, and this success is largely due to their flight ability. Interestingly, some stick insects have lost their flight ability despite having wings. To elucidate the shift from wingless to flying forms during insect evolution, we compared the nutritional metabolism system among flight-winged, flightless-winged, and flightless-wingless stick insect groups.
Results
Here, we report RNA sequencing of midgut transcriptome of Entoria okinawaensis , a prominent Japanese flightless-wingless stick insect, and the comparative analysis of its transcriptome in publicly available midgut transcriptomes obtained from seven stick insect species. A gene enrichment analysis for differentially expressed genes, including those obtained from winged vs wingless and flight vs flightless genes comparisons, revealed that carbohydrate metabolic process-related genes were highly expressed in the winged stick insect group. We also found that the expression of the mitochondrial enolase superfamily member 1 transcript was significantly higher in the winged stick insect group than in the wingless stick insect group. Our findings could indicate that carbohydrate metabolic processes are related to the evolutionary process through which stick insects gain the ability of flight.
... Lipid and protein are considered to be the main compounds required for development of the embryo (Beenakkers et al., 1981); for example, in Culex quinquefasciatus (Diptera: Culicidae) (Van Handel, 1993). Lipid forms 30-40% of dry ovary weight in several insect species (Allais et al., 1964;Troy et al., 1975;Kawooya & Law, 1988;Briegel, 1990;Ziegler & Van Antwerpen, 2006). ...
Insects with access to finite energy resources must allocate these between maintenance and reproduction in a way that maximizes fitness. This will be influenced by a range of life‐history characteristics and the environment in which any particular insect species lives. In the present study, females of the blowfly Lucilia sericata (Diptera: Calliphoridae) were fed diets differing in protein and carbohydrate (sucrose) content and the allocation of lipid to reproduction was quantified using a spectrophotometric method of analysis. Immediately after adult emergence, total body lipid, scaled for differences in body size, showed an initial decline as it was utilized to meet the metabolic demands of cuticle deposition, muscle maturation and then flight. When flies were denied access to sucrose, stored lipid then continued to decrease until flies died, usually within 4 days of emergence. However, flies given access to sucrose were able to increase body lipid content, demonstrating that carbohydrate is essential for homeostasis and that it can be used to synthesize lipid. Nevertheless, female flies fed sucrose only were unable to synthesize egg yolk. Only flies provided with protein were able to mature eggs. However, the rate of egg maturation and number and size of eggs matured were greater for female flies given liver compared with flies provided with pure whey protein powder. The results demonstrate the importance of different dietary components for different elements of the life‐history of L. sericata, namely survival and reproduction. Blowflies denied access to sucrose died within 4 days of emergence even when provided with protein. Only blowflies provided with sucrose plus protein were able to mature eggs. Carbohydrate is essential for blowfly survival and protein is essential for egg production.
... MSI can characterize the spatial and temporal distributions of various molecules on the surface of biological tissue samples, including small molecules (e.g., lipids) and macromolecules (e.g., peptides and proteins). Lipids play a fundamental role in a number of biological functions, such as maintenance of cell membrane structure, energy storage, intracellular and extracellular signaling, insect pheromones, chemical communication, and social behavior (Beenakkers, van der Horst, & van Marrewijk, 1981;Gilbert & Chino, 1974). D. melanogaster, as a biological model insect, has been widely used in many perspectives of MSI, such as three-dimensional spatial distribution of neutral lipids on the surface of adults (Kaftan et al., 2014), lipid distribution in the body (Niehoff et al., 2014), lipid structure in brain (Le et al., 2018;Phan, Munem, Ewing, & Fletcher, 2017), lipids of the wing (Marty et al., 2017;Vrkoslav, Muck, Cvačka, & Svatoš, 2010), and phospholipid distribution of the malpighian tubules (E. ...
Mass spectrometry imaging (MSI) can visualize the composition, abundance, and spatial distribution of molecules in tissues or cells, which has been widely used in the research of life science. Insects, especially the agricultural pests, have received a great deal of interests from the scientists in biodiversity and food security. This review introduces the major characteristics of MSI, summarizes its application to the investigation of insect endogenous metabolites, exogenous metabolites, and the spatiotemporal changes of metabolites between insects and plants, and discusses its shortfalls and perspectives. The significance of these concerns is beneficial for future insect research such as physiology and metabolism.
Research Highlights
• Mass spectrometry imaging (MSI) is an emerging technology applied into insect research fields to illuminate the spatiotemporal changes of metabolites.
• MSI could be further optimized and expand its application range of insect physiology and metabolism research.
... In locusts, for example, for the first 10-15 min of flight, carbohydrate is the primary fuel source during which they fly at high speed (Goldsworthy et al., 1979). After this period, locusts slow down to a 'cruising speed' and the flight muscles switch to oxidising the higher-energy content found in lipids with 1 mg of lipid creating as much energy as 8 mg of glycogen (Beenakkers et al., 1981). A number of flight mill studies have demonstrated that other insects also use lipids as the primary migratory fuel (Vanhandel, 1974;Teo et al., 1987;Sappington et al., 1995;Kent et al., 1997;Murata & Tojo, 2004). ...
1. Every year billions of insects engage in long‐distance, seasonal mass migrations which have major consequences for agriculture, ecosystem services and insect‐vectored diseases. Tracking this movement in the field is difficult, with mass migrations often occurring at high altitudes and over large spatial scales.
2. As such, tethered flight provides a valuable tool for studying the flight behaviour of insects, giving insights into flight propensity (e.g. distance, duration and velocity) and orientation under controlled laboratory settings. By experimentally manipulating a variety of environmental and physiological traits, numerous studies have used this technology to study the flight behaviour of migratory insects ranging in size from aphids to butterflies. Advances in functional genomics promise to extend this to the identification of genetic factors associated with flight. Tethered flight techniques have been used to study migratory flight characteristics in insects for more than 50 years, but have never been reviewed.
3. This study summarises the key findings of this technology, which has been employed in studies of species from six Orders. By providing detailed descriptions of the tethered flight systems, the present study also aims to further the understanding of how tethered flight studies support field observations, the situations under which the technology is useful and how it might be used in future studies.
4. The aim is to contextualise the available tethered flight studies within the broader knowledge of insect migration and to describe the significant contribution these systems have made to the literature.
... Recent molecular studies have shown that high density Lp (HDLp) is the one endocytosed as an intact particle by the cell surface Lp receptors (LpRs) [21][22][23][24][25]. After endocytosis, the neutral lipids are hydrolyzed from lipoprotein`s core by lysosomal digestion and are stored as lipid droplets in the oocyte for future energy source of the developing embryo [26][27][28]. ...
The embryonic development of all oviparous animals occurs isolated from the maternal body. The egg should therefore contain all necessary supplies for the development of the embryo until eclosion. This supply is called yolk and is composed of nucleic acids, proteins, lipids and carbohydrates, stored in an organized manner inside the egg. Most of the yolk protein components are taken up during oocyte development via receptor-mediated endocytosis. Major proteins accumulated by insect oocytes are the two hemolymph lipoproteins, vitellogenin (Vg) and lipophorin (Lp). Once sequestered, the Vg is sent to yolk bodies for processing and stored as vitellin (Vn), the main nutritional reserves for the future embryo, whereas Lp (the high density Lp, HDLp) after unloading lipids (which are stored as lipid droplets, the energy source for the embryo) is stored as a very HDLp (VHDLp). This chapter reviews the current state of knowledge on the major yolk protein precuros (YPPs), the Vg and Lp, in insects and their role in oogenesis. Besides the biochemical and molecular aspects, the hormonal regulation and the uptake mechanism of these YPPs by the developing oocytes through receptor-mediated endocytosis will be addressed. Also, we point out some of the important areas for future research.
The diazepam-binding inhibitor (DBI; also called acyl coenzyme A-binding protein or endozepine) is a 10-kDa polypeptide found in organisms ranging from yeasts to mammals. It has been shown that DBI and its processing products are involved in various specific biological processes such as GABAA/benzodiazepine receptor modulation, acyl coenzyme A metabolism, steroidogenesis, and insulin secretion. We have cloned and sequenced the Drosophila melanogaster gene and cDNA encoding DBI. The Drosophila DBI gene encodes a protein of 86 amino acids that shows 51 to 56% identity with previously known DBI proteins. The gene is composed of one noncoding 5' and two coding exons and is localized on the chromosomal map at position 65E. Several transcription initiation sites were detected by RNase protection and primer extension experiments. Computer analysis of the promoter region revealed features typical of housekeeping genes, such as the lack of TATA and CCAAT elements. However, in its low GC content and lack of a CpG island, the region resembles promoters of tissue-specific genes. Northern (RNA) analysis revealed that the expression of the DBI gene occurred from the larval stage onwards throughout the adult stage. In adult flies, DBI mRNA and immunoreactivity were detected in the cardia, part of the Malpighian tubules, the fat body, and gametes of both sexes. Developmentally regulated expression, disappearing during metamorphosis, was detected in the larval and pupal brains. No expression was detected in the adult nervous system. On the basis of the expression of DBI in some but not all tissues with high energy consumption, we propose that in D. melanogaster, DBI is involved in energy metabolism in a manner that depends on the substrate used for energy production.
The study evaluated the effects of R-limonene, in sublethal concentration, on the histology, histochemistry, biochemistry, and carbohydrates and proteins levels in the third instar Aedes aegypti larvae. The R-limonene (LC50 of 27 ppm) and control groups were analyzed 12 and 24h after the beginning of treatments. The midgut of the control larvae was composed of cylindrical and elongated cells with a spherical and central nucleus and regenerative cells with a pyramidal shape. After 12 hours of treatment, columnar cells, protuberances, and cytoplasmic vacuolization were found. However, 24 hours after treatment, complete disorganization of the epithelium was observed. There was a positive reaction in all treatments for the presence of glycogen. However, the midgut of larvae treated with R-limonene showed higher levels. For the total protein, positive marking occurred in all groups evaluated, with higher levels in treatments and the lowest in control 12h. The levels of total protein and glycogen increased in the treated larvae compared to the 12h control. Besides, a reduction in total sugar levels was observed in the treated larvae compared to controls 12 and 24h, being more evident in the last one. Therefore, these results demonstrate that R-Limonene caused pathological changes in the epithelium of the A. aegypti midgut at histophysiological and biochemical levels.
Research regarding the distribution of metabolites is a vital aspect of insect molecular biology. However, current approaches (e.g., liquid chromatography-mass spectrometry or immunofluorescence) have cons like requirement of massive tissues, low efficiency, and complicated operating processes. As an emerging technology, mass spectrometry imaging (MSI) can visualize the spatiotemporal distribution of molecules in biological samples without labeling. In this chapter, we retrospect the major types of in situ measurement by MSI, and the application of MSI for investigating insect endogenous and exogenous metabolites and monitoring the dynamic changes of metabolites involved with the interactions between insects and plants. Future studies that combine MSI with other genetic tools can facilitate to better explore the underlying mechanisms concerning insect physiology and metabolism.
Allatectomy has no apparent effects upon feeding activity in males of L. m. migratorioides. If allatectomized locusts are forced to take vigorous exercise, food consumption is increased slightly. Allatectomized males exhibit active sexual behaviour, although they do not develop a mature coloration. The accumulation of lipid in allatectomized males can be limited by forcing the insects to take vigorous exercise. The possibility that hypertrophy of the fat body is due to lethargy in allatectomized male locusts is discussed but considered to be unlikely.
This chapter explores the various physiological and biological changes occurring in an insect's body during the various stages of the insect's development. Insects taken together as a group exhibit a continuing series of physiological transformations. This includes the most fundamental courses of events, for example, the regulatory capacity of the egg and the degree of metamorphosis the insect undergoes nearing full maturity. The cleidoic insect egg represents a closed system, and embryonic development is completed with greater independence from environmental factors providing a great opportunity to study early developments in physiology of insect. There is also a close correspondence between embryonic determination and quantity of periplasm. During oogenesis, the insect egg grows considerably through the deposition of yolk. Thus, the egg nucleus occupies only a very small fraction of the egg volume, often located in the anterior half of the egg and surrounded by a small island of cytoplasm. The inner structure of the insect egg may show certain stratification. When the juvenile form has a demand for the same food as the adult, the postembryonic changes are only gradual through a series of molting. If there are great differences between the larval and adult requirements for nutriment and habitat, the corresponding difference in the organization type of the larva and imago has to be covered by some rather profound processes of metamorphosis.
Publisher Summary This chapter analyzes the metabolic events that are fundamental to the transition of a muscle from a controlled resting state to one so active that energy transformations are taking place at a rate far in excess of that for any other biological process. The approach has been to identify the enzymatic reactions that are facilitated during the transition, to determine the mechanisms of activation at each locus of control, and then to formulate a working hypothesis that will unite the experimental findings into an overall scheme for the metabolic regulation of the tissue. Many of the experimental observations have been made with isolated enzymes and subcellular organelles. Thus, the in vivo environment can never be adequately reconstructed. Moreover, knowledge of the metabolite levels permitting simulation of in vivo conditions assumes uniform distribution of these substances and excludes compartmentation. These reservations made, the sites of regulation in fly flight muscle have been identified by measuring coincident and sequential changes in the concentrations of the metabolic intermediates.
This chapter reviews the influence that endocrine hormones have on the growth and development of insects. The mechanism of action of none of the insect hormones is known with certainty, and it is postulated that they may act at several of the many possible control points. As several orders of insects are separated widely in evolutionary time, it might be that growth hormones do not act uniformly in all insects. The classical scheme of endocrine control of molting and metamorphosis in holometabolous insects has been plagued by questions raised as a result of contemporary investigations in the functioning of insect hormones. An exception to the classical scheme is the finding that renewed secretion by the brain is not always needed for each molt. Insect neurosecretory cells appear to play important roles in many other physiological processes. One important question that needs answering relates to the regulation and mechanism of synthesis and release of neurosecretion in insect cells. The activity of α-ecdysone—arthropod hormones that are produced by the prothoracic gland in insects and that trigger molting and metamorphosis and are synthesized from chiolestrol—and various side chain deoxyecdysones is partially because of their metabolism to β-ecdysone.
The intensity and precise control of metabolic processes in the flight muscle of insects during flight have engaged the attention of biochemists and physiologists for many years. The over-all level of metabolism in the working muscle may be estimated from either the depletion of the animals’ depots of fuel or the respiratory exchange. Values as high as 2400 cal/g muscle/h for the bee during prolonged periods of continuous flight have been reported (Weis-Fogh, 1952). This value is 30- to 50-fold those for leg and heart muscle of man at maximum activity. With respect to the utilization of energy reserves, it has been found that the locust during flight consumes fat at a rate of 4.1 mg per h (Beenakkers, 1965). The cost of flight in insects becomes fully evident from a comparison of the rate of oxygen uptake during flight with that of the same insect at rest. On initiation of flight, some blowflies consume oxygen at a rate of about 3000 µl/min/g, elevating their basal rates approximately 100-fold (Davis and Fraenkel, 1940). This is the most intense respiration known in biology and also the most controlled. By contrast, the respiration of humming birds in flight, although much greater per unit weight than that recorded for any other vertebrate, is subject to a control of only 5-fold (Pearson, 1950). From these few selected examples, and others reported elsewhere (Sacktor, 1965, 1970), it is apparent that insect flight muscle is the tissue of choice for the study of the control of catabolism and biological oxidations, and many of the results obtained with insects have a significance and a relevance which transcend the boundaries between classes.