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    Antagonists and defense mechanisms of entomopathogenic nematodes and their mutualistic bacteria
    (Academic Press Inc Elsevier Science, 2021) Raja, Ramalingam Karthik; Arun, Alagarsamy; Touray, Mustapha; Gulsen, Sebnem Hazal; Cimen, Harun; Gulcu, Baris; Hazir, Selcuk
    Entomopathogenic nematodes (EPNs) in the families Steinernematidae and Heterorhabditidae are effective biocontrol agents against a number of important soil insect pests and are safe to vertebrates, plants and other non-target organisms with no negative effects on the environment. They are associated with mutualistic bacteria in the genus Xenorhabdus for Steinernematidae and Photorhabdus for Heterorhabditidae and are often referred to as the nematode/bacterium complex. The natural habitat of EPNs is the soil where the third-stage infective juveniles (IJs), the only free-living stage, can infect an array of insect hosts. However, the survival of the IJs is affected by various abiotic (i.e., temperature, moisture, soil texture, soil salinity, UV light, oxygen, and pH) and biotic (i.e., natural enemies, omnivores, scavengers, competitors, and plants) factors in the soil. In this review, we summarize the impact of the biotic factors, especially natural enemies, omnivores, scavengers, and competitors against EPNs and conclude that the major predators of the IJs appear to be nematophagous fungi, mites, and collembolans. Omnivores and scavengers, particularly, mites, collembolans, ants and birds, feeding on EPNkilled insects appear to be the major mortality factors on the developing nematodes especially of insects that are 2 days or less post infection. In addition, we discuss the defense mechanisms of EPN IJs against nematophagous fungi, and the protection of the nematode-killed insects by production of the scavenger deterrent factor produced by the mutualistic bacteria against omnivores and scavengers. By understanding the interactions between EPNs and their antagonists we can improve and increase the successful use of EPNs in biological control programs.
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    Response of three cyprinid fish species to the Scavenger Deterrent Factor produced by the mutualistic bacteria associated with entomopathogenic nematodes
    (Academic Press Inc Elsevier Science, 2017) Raja, Ramalingam Karthik; Aiswarya, Dilipkumar; Gülcü, Barış; Raja, Manickam; Perumal, Pachiappan; Sivaramakrishnan, Sivaperumal; Hazır, Selçuk
    The symbiotic bacteria, Photorhabdus and Xenorhabdus associated with entomopathogenic nematodes (EPNs) in the genera Heterorhabditis and Steinernema, respectively, produce a compound(s) called the Scavenging Deterrent Factor (SDF). SDF deters a number of terrestrial insect scavengers and predators and one bird species from feeding on host insects killed by the nematode-bacterium complex but has not been tested against aquatic vertebrates. Moreover, the Heterorhabditis-Photorhabdus association is believed to have evolved in an aquatic environment. Accordingly, we hypothesized that SDF will deter fish from feeding on nematode-killed insects and tested the responses of three omnivorous fresh water fish species, Devario aequipinnatus, Alburnoides bipunctatus, and Squalius pursakensis, to SDF in the laboratory. When the fish were exposed to Galleria mellonella larvae killed by the Heterorhabditis- or Steinernema-bacterium complex at 2 or 4 days post-infection, all three fish species made several attempts to consume the cadavers but subsequently rejected them. However, all fish species consumed freeze killed control larvae. In a choice test, when D. aequipinnatus or A. bipunctatus were offered a pair of nematode-killed larvae, both fish species rejected these cadavers; when offered a nematode-killed larva and a freeze-killed larva, both fish species consumed the freeze-killed larva but not the nematode-killed one. In further tests with D. aequipinnatus, there was no significant difference in the number of 2-day-old Bacillus thuringiensis subsp. kurstaki-killed (Btk) larvae consumed compared to freeze-killed larvae, but significantly fewer 4-day-old Btk-killed larvae were consumed compared to freeze-killed larvae. When D. aequipinnatus was fed G. mellonella larvae killed by the symbiotic bacteria, the fish rejected the cadavers. When given freeze-killed or nematode-killed mosquito (Aedes aegypti) larvae, the fish consumed significantly more of the former larvae (99%) compared to the latter (55%). When D. aequipinnatus was placed in a symbiotic cell-free supernatant for 18 h, a significant reduction in consumption of freeze killed larvae compared to cell-free Btk or control broth supernatant was observed. We showed that SDF protects the nematode-killed insects from being consumed by omnivorous fishes and suggests that they will have minimal effects on recycling of EPNs in the aquatic environment. (C) 2016 Elsevier Inc. All rights reserved.