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 A₂ 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.

Keywords: PLA2; Photorhabdus; Spodoptera; eicosanoid; immunity; pathogenicity.