Lipids as a key element of insect defense systems

Abstract

The relationship between insect pathogenic fungi and their insect hosts is a classic example of a co-evolutionary arms race between pathogen and target host: parasites evolve towards mechanisms that increase their advantage over the host, and the host increasingly strengthens its defenses. The present review summarizes the literature data describing the direct and indirect role of lipids as an important defense mechanism during fungal infection. Insect defense mechanisms comprise anatomical and physiological barriers, and cellular and humoral response mechanisms. The entomopathogenic fungi have the unique ability to digest the insect cuticle by producing hydrolytic enzymes with chitin-, lipo- and proteolytic activity; besides the oral tract, cuticle pays the way for fungal entry within the host. The key factor in insect resistance to fungal infection is the presence of certain types of lipids (free fatty acids, waxes or hydrocarbons) which can promote or inhibit fungal attachment to cuticle, and might also have antifungal activity. Lipids are considered as an important source of energy, and as triglycerides are stored in the fat body, a structure analogous to the liver and adipose tissue in vertebrates. In addition, the fat body plays a key role in innate humoral immunity by producing a range of bactericidal proteins and polypeptides, one of which is lysozyme. Energy derived from lipid metabolism is used by hemocytes to migrate to the site of fungal infection, and for phagocytosis, nodulation and encapsulation. One polyunsaturated fatty acid, arachidonic acid, is used in the synthesis of eicosanoids, which play several crucial roles in insect physiology and immunology. Apolipoprotein III is important compound with antifungal activity, which can modulate insect cellular response and is considered as important signal molecule.

Keywords: arachiadonic acid metabolites; cuticle; fungal infection; hemocyte; insect defense mechanisms; lipid.

FIGURE 1

Lipid metabolism in insects. Lipids are digested at the midgut lumen and then absorbed and metabolized by midgut cells. Subsequently, they are transported in the hemolymph by lipophorin to fat body and oocytes, where they are stored in lipid droplets. Abbreviations: CE, Cholesteryl ester; Cho, Cholesterol; DAG, diacylglycerol; FFA, Free fatty acid; LD, Lipid droplet; Lp, Lipophorin; LPL, Lysophospholipid; LpR, Lipophorin receptor; PL, Phospholipid; TAG, triacylglycerol (based on the information in Majerowicz and Gondim (2013); structural formulas of chemical compounds from PubChem database).

FIGURE 2

Overview of the role of lipids during infection in insects. Parts of the figure were drawn by using pictures from Servier Medical Art. Servier Medical Art by Servier is licensed under a Creative Commons Attribution 3.0 Unported License.

FIGURE 3

The ecdysteroid biosynthesis pathway in the prothoracic gland and the role of 20 dehydroecdysone in insect immunity. Cholesterol is converted into 20-dehydroecdysone (20E) by several ecdysteroidogenic enzymes (red font). Ecdysteroid biosynthesis starts from the conversion of cholesterol to 7-dehydrocholesterol (7 dC). Then, 7 dC is converted to ketodiol via multiple steps with the participation of a group of enzymes called “Black Box.” In the terminal catalytic steps of ecdysteroid biosynthesis, ketodiol is then sequentially hydroxylated at carbon 25, carbon 22, carbon 2, and lastly carbon 20, resulting in a conversion to the active steroid hormone 20E (based on the information in Niwa and Niwa (2014), Saito et al. (2016), Chanchay et al. (2019); structural formulas of chemical compounds from PubChem database).

FIGURE 4

Eicosanoid biosynthesis and degradation in insects. Phospholipase A2 (PLA2) catalyzes the hydrolysis of linoleic acid (LA) from membrane-associated phospholipids (PLs); the resulting LA is elongated by long-chain fatty acid elongase (Elo) and then desaturated by desaturase (Des) to arachidonic acid (ARA). ARA is then oxygenated by epoxidase (EPX) into epoxyeicosatrienoic acid (EET), lipoxygenase (LOX) into leukotriene (LT), or cyclooxygenase-like peroxynectin (Pxt) to prostaglandin (PG). The EETs are degraded by soluble epoxide hydrolase (sEH). LTA4 is formed from 5-hydroxyperoxide eicosatetraenoic acid (HpETE) and changed into LTB4 by LTA4 hydrolase (LTA4H) or into LTC4 by glutathione peroxidase (Gpx). Finally, various PGs are formed from PGH2 by cell-specific enzymes, thromboxane A2 (TXA2) synthase (TXAS), PGD2 synthase (PGDS), PGE2 synthase (PGES), and PGI2 synthase (PGIS); these PGs are degraded by PG dehydrogenase (PGDH) and PG reductase (based on the information in Kim and Stanley (2021); structural formulas of chemical compounds from PubChem database; part of the figure were drawn by using pictures from Servier Medical Art. Servier Medical Art by Servier is licensed under a Creative Commons Attribution 3.0 Unported License).