Eicosanoid mediation of immune responses at early bacterial infection stage and its inhibition by Photorhabdus temperata subsp. temperata, an entomopathogenic bacterium

Abstract

An entomopathogenic bacterium Photorhabdus temperata subsp. temperata (Ptt) infects insect hemocoel by the vectoring activity of its symbiotic nematode, Heterorhabditis megidis. The bacterium induces host immunosuppression by inhibiting eicosanoid biosynthesis. This study investigated the role of eicosanoids in immune responses of the beet armyworm, Spodoptera exigua, in the early bacterial infection stage (first 3 hr postinfection [PI]). After infection with the nonpathogenic Escherichia coli (Ec), the bacterium maintained its population for the first 3 hr PI, then rapidly decreased in numbers. During the 3 hr PI of Ptt, this pathogenic bacterium also did not show any significant change in bacterial population. However, Ptt rapidly increased its population size after the initial lag phase, inducing fatal septicemia. This study further analyzed cellular and humoral immune responses of the beet armyworm during the initial 3 hr PI. During this early stage, challenge with Ec stimulated hemocyte-spreading behavior along with extensive F-actin growth. However, Ptt infection suppressed hemocyte spreading. Expression levels of three antimicrobial peptides (lysozyme, gloverin, and gallerimycin) were significantly inhibited during Ptt infection. Phospholipase A activity was significantly induced during the early infection stage of Ec, but not during Ptt infection. Addition of eicosanoid biosynthesis inhibitors significantly reversed the initial immunosuppression. These results suggest that, during the early infection stage, Ptt can shutdown eicosanoid biosynthesis which can prevent acute immune responses of host insects.

Dual Oxidase-Derived Reactive Oxygen Species Against Bacillus thuringiensis and Its Suppression by Eicosanoid Biosynthesis Inhibitors

“…Two entomopathogenic bacterial genera, Xenorhabdus and Photorhabdus, can inhibit target insect immune responses by inhibiting eicosanoid biosynthesis through inhibition of PLA 2 activity with their secondary metabolites (Kim et al, 2005). However, most analyses of immunosuppression have been focused on cellular and humoral immunity in hemocoel because bacteria can infect and multiply in the insect hemocoel (Kim et al, 2018a). Several studies have shown that Bt pathogenicity can be enhanced by the addition of bacterial culture broth or metabolite compounds (Jung and Kim, 2007;Kwon and Kim, 2008).…”

“…Cellular immune responses include hemocyte-mediated phagocytosis, encapsulation, and nodule formation via activating hemocytespreading behavior (Ahmed and Kim, 2019). Humoral immune responses are executed by various antimicrobial peptides (AMPs) and activated at relatively later stage of infection to remove the remaining microbes after activating cellular immunity (Haine et al, 2008;Kim et al, 2018a).…”

Virulent secondary metabolites of entomopathogenic bacteria genera, Xenorhabdus and Photorhabdus, inhibit phospholipase A2 to suppress host insect immunity

“…Protein toxins that also induce the immunosuppression and nally kill target insects are known in Xenorhabdus and Photorhabdus [25]. However, acute attack by a target insect's immune system should be avoided and actively suppressed by the secondary metabolites [26].…”

Virulent Secondary Metabolites of Entomopathogenic Bacteria, Xenorhabdus and Photorhabdus, Inhibit PLA2 to Suppress Host Insect Immunity

“…Protein toxins that can kill target insects are known in Xenorhabdus and Photorhabdus [25]. However, acute attack by a target insect's immune system should be avoided and actively suppressed by the secondary metabolites [26].…”