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Microbial Toxins in Insect/Nematode Biocontrol
Invertebrate pests, such as insects and nematodes, not only cause or transmit human and livestock diseases but also impose serious crop losses by direct injury as well as vectoring pathogenic microbes. This is amply demonstrated by the successful and widespread use of Bacillus thuringiensis (Bt) to control mosquitos and many plant pests, the latter by the transgenic expression of Bt-insecticidal proteins in crop plants. Identifying as well as characterizing the molecular nature and regulation of the biocidal activity has led to the enormous success of Bt as a biocontrol agent, which serves as a great model for advancing nascent biocontrol agents into commercial products.
Insects constitute the largest and most diverse group of animals (~2.5 million species) on Earth . With the exception of a few beneficial insects such as pollinators, they form the costliest animal group to human society by spreading devastating infectious diseases in humans, livestock and crops, ravaging food stocks, damaging forests, destroying infrastructure and weakening the resilience of ecosystems . The Nematoda (also called Nemathelminthes), with an estimated 500,000 species, is the second largest phylum in the animal kingdom . Most species of nematodes are either innocuous or play beneficial ecological and agronomic roles, by nutrient recycling and controlling insects and other harmful nematodes . At the same time, some nematodes cause serious diseases in plants, humans and other animals.
Biocontrol is the means of controlling pests and pathogens through the use of other organisms, which can be natural enemies, such as predators, parasitoids, pathogens and competitors. It is an environmentally safe, low-cost and effective approach and occurs in natural communities. Much before the introduction of chemical pesticides, biocontrol has been in practice to control agricultural pests, with the first recorded report in 304 AD from China .
2. Pore-Forming Toxins
Pore-forming toxins (PFTs) are the largest class of proteinaceous bacterial toxins and important virulence factors, such as colicins of E. coli and anthacin of anthrax. All PFTs are synthesized as water-soluble proteins but subsequently become membrane bound. They recognize host cells based on specific cell surface receptors, which can be proteins, lipids or sugars. The binding allows a rapid increase in the local concentration of a PFT and its oligomerization, which is followed by insertion and pore formation in the host cell membrane. The changes in the permeability of the membrane due to pore formation depends on the toxin, ranging from the loss of small ions, e.g., K+ and Ca2+, to macromolecules such as proteins .
B. thuringiensis (Bt, hereafter) was first isolated in Japan in 1902 from dead silkworm (Bombyx mori) larvae and soon recognized as an entomopathogenic bacterium. Bt was one of the first prokaryotic BCAs used as a commercial insecticide in France in 1938 . The insect- and nematode-specific pathogenicity of Cry toxins is due to their oral toxicity, and these toxins are active against a wide range of insects from Lepidoptera, Coleoptera, Hymenoptera and Diptera, as well as nematodes .
3. Insect Ion Channel Modulators
Ion channel modulators have clear advantages as pesticidal targets in that they act quickly and allow the rapid reduction of insect pressure. Five ion channels within the insect nervous system have been the primary targets for the development of small molecule insecticides and also serve as effective targets for biopesticides. These are the γ-aminobutyric acid (GABA) receptor, the glutamate-gated chloride channel, the nicotinic acetylcholine receptor or nAChR, the voltage-gated sodium channel and the ryanodine receptor .
Nodulisporic acid A, a natural insecticidal indole terpene isolated from an endophytic fungus, Nodulisporium sp., also inhibits only invertebrate-specific glutamate-gated chloride (Glu-Cl) channels . Based on its safety, Merck & Co. introduced synthetic versions of the compound as a potent oral formulation to control fleas and ticks in dogs and cats . Ryanodine receptors (RyRs) belong to a group of ligand-gated calcium channels initially reported from vertebrates. They are located on the endoplasmic reticulum of muscle cells and neurons and play a critical role in muscle contraction. In contrast to mammals, which have three types of RyRs, insects have only a single RyR, which is a major target for modern insecticides. Ryanodine, a plant alkaloid and an important ligand of RyR, has served as a natural botanical insecticide. Attempts to generate synthetic commercial analogs of ryanodine have, so far, not succeeded. Despite the popularity of diamide insecticides due to their specificity, several agricultural pests have become resistant to the chemical insecticides due to mutations in a transmembrane region of their RyRs , and there is a need for alternative RyR agonists. Cyclodepsipeptides are a large family of peptide-related natural products with an α-hydroxy acid and 5–10 amino acids linked by amide and ester bonds . Verticilide, a cyclooctadepsipeptide produced by Verticillium sp. FKI-1033, has been shown to bind selectively to the insect ryanodine receptor in the low micromolar range .
4. Innate Immunity Busters
Insects, like all invertebrates, express both innate and humoral immunity to infection. Biological control strategies that are targeted to these pathways have a great potential for success.
Bacteria belonging to 24 species of Xenorhabdus and five of Photorhabdus are known worldwide for their entomopathogenic potential. Some species (e.g., P. luminescens and X. nematophila) have mutualistic associations with nematodes and share their entomophagous lifestyle. The soil-dwelling entomopathogenic nematode larvae find and penetrate the insect larvae through natural openings and release symbiotic bacteria into the insect hemocoel. The bacteria replicate in the insect body and release immuno-suppressive toxins. At least seven secondary metabolites that inhibit PLA2, namely, benzylideneacetone (BZA), proline-tyrosine, acetylated phenylalanine-glycine-valine, indole, oxindole, cis-cyclo-PY and p-hydroxyphenyl propionic acid, have been reported. They also show significant inhibitory activities against other immune responses, such as phenoloxidase activity (PO) and hemocytic nodulation, with BZA being the most effective . An isocyanide-containing compound rhabducin produced by Xenorhabdus can also inhibit phenoloxidase and thereby melanization . In addition, phurealipids (urea compounds) made by these bacteria can prevent the expression of antimicrobial peptide genes in the insect hosts, a part of the humoral component of immunity .
5. Cyclic Lipopeptide Surfactants
Cyclic lipopeptides (CLPs) are amphiphilic molecules composed of a cyclic oligopeptide lactone ring coupled to a fatty-acid tail. Their structural diversity and cyclic configuration confer them with broad-spectrum and environmentally stable antibiosis activity against bacteria, fungi, insects, protozoa and even human tumor cell lines . CLPs are produced mostly by Pseudomonas, Bacillus and Streptomyces spp. CLPs come in three families, namely surfactin, iturin and fengycin, and a single strain can make one or more of them contribute to varying biocidal activities. Pseudomonad spp. (e.g., P. chlororaphis, P. fluorescens, P. protegens, P. putida, P. mosselli and P. entomophila) are particularly pathogenic toward insects and nematodes.
6. Psychoactive Compounds
Many microbial parasites manipulate host insect behavior for the enhanced dispersal of their inoculum and thereby spread disease. A few of them, such as baculoviruses, hijack host genes involved in insect physiology , whereas others make their own . Many entomopathogenic fungi cause “summit disease” (SD) behavior, an extended phenotype where parasitized insects ascend and affix to elevated substrates prior to death. For example, the fungal pathogen Entomophthora muscae infects wild Drosophila and manipulates host behavior . This facilitates a wider dissemination of fungal spores from the mummified insect carcasses. It is speculated that E. muscae may produce and secrete eicosanoid-like compounds to induce behavioral changes in the dying host . More details are available about the bizarre behavior in cicadas induced by the pathogenic fungi Massospora and Strongwellsea. M. cicadina, M. platypediae, M. levispora, S. tigrinae and S. acerosa keep their insect hosts alive while sporulating, which enhances dispersal via sexual transmission.
More research is needed to validate the findings from -omics analyses to unequivocally implicate any of these putative chemosignaling compounds in insect behavioral manipulation. Nevertheless, this concept has been successfully exploited in the management of some pests, e.g., codling moth (Cydia pomonella, a key insect pest of apple), using host endogenous molecules, especially pheromones .
8. Sterol Homeostasis Disruptors
9. Uncouplers and Electron Transport Inhibitors
The entry is from 10.3390/ijms22147657
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