Specific immune priming in the invasive ctenophore Mnemiopsis leidyi

Abstract

Specific immune priming enables an induced immune response upon repeated pathogen encounter. As a functional analogue to vertebrate immune memory, such adaptive plasticity has been described, for instance, in insects and crustaceans. However, towards the base of the metazoan tree our knowledge about the existence of specific immune priming becomes scattered. Here, we exposed the invasive ctenophore Mnemiopsis leidyi repeatedly to two different bacterial epitopes (Gram-positive or -negative) and measured gene expression. Ctenophores experienced either the same bacterial epitope twice (homologous treatments) or different bacterial epitopes (heterologous treatments). Our results demonstrate that immune gene expression depends on earlier bacterial exposure. We detected significantly different expression upon heterologous compared with homologous bacterial treatment at three immune activator and effector genes. This is the first experimental evidence for specific immune priming in Ctenophora and generally in non-bilaterian animals, hereby adding to our growing notion of plasticity in innate immune systems across all animal phyla.

An evolutionary comparative analysis of the medusozoan (Cnidaria) exoskeleton

“…Yet, Chs genes have not been found in the genomes of nonchitinous organisms (Willmer, ; Wagner, ), e.g. Trichoplax adhaerens Schulze, 1883 (Placozoa; Dellaporta et al ., ; Signorovitch, Buss & Dellaporta, ) and Mnemiopsis leidyi A. Agassiz, 1865 (Ctenophora; Table ; Ryan et al ., ; Bolte et al ., ).…”

Recent advances in vertebrate and invertebrate transgenerational immunity in the light of ecology and evolution

“…Despite lacking the characteristic antibody-mediated immune memory achieved by the adaptive immune system in vertebrates, invertebrates have been shown to exhibit functionally analogous responses to immune memory, which provides increased protection on secondary pathogen/parasite exposures. The breadth of taxa with some form of this immune memory-like response is impressive, from comb jellies (Bolte et al 2013), sea anemones (Brown and Rodriguez-Lanetty 2015) and bivalves, through a variety of crustaceans (Rowley and Pope 2012) and insects (Sadd and Schmid-Hempel 2006;Roth et al 2009), spanning >900 million years of divergence. For within generational immune priming in diverse invertebrates we refer readers to a recent and thorough review of the topic (Milutinović and Kurtz 2016).…”

The modulation of extracellular superoxide dismutase in the specifically enhanced cellular immune response against secondary challenge of Vibrio splendidus in Pacific oyster (Crassostrea gigas)

“…A significant down-regulation of CgEcSOD was revealed after the secondary V. splendidus stimulation by both real-time PCR and western-blot, indicating that the deduction of CgEcSOD should be a strategy responding to the secondary challenge. Likewise, recent reports in ctenophore evidenced that the expression of superoxide dismutase (Cu-Zn SOD) was reduced upon homologous bacterial challenge but not for the heterologous (Bolte et al, 2013). Although EcSOD was though to protect tissues from over expressed ROS production, its inhibition on innate immune response was also reported (Edwards et al, 2001;Witter et al, 2014).…”

“…Similarly, the downregulation of EcSOD after the repeat immune challenge also suggested its important role during the specific immune priming (Bolte et al, 2013). For example, extracellular Cu-Zn SOD in ctenophore was down-regulated after a secondary homologous bacterial challenge, which was inferred as a tactics to reduce inflammatory response, saving resources and cutting down selfdamage (Bolte et al, 2013). Specifically cellular immune priming was also reported in the oysters upon the secondary challenge of live V. splendidus (Zhang et al, 2014).…”

“…The mechanism underlying this confliction is still obscure and it has been speculated as a particular strategy to benefit the host of surviving from the invasion of V. aestuarianus 01/32 (Labreuche et al, 2006). Similarly, the downregulation of EcSOD after the repeat immune challenge also suggested its important role during the specific immune priming (Bolte et al, 2013). For example, extracellular Cu-Zn SOD in ctenophore was down-regulated after a secondary homologous bacterial challenge, which was inferred as a tactics to reduce inflammatory response, saving resources and cutting down selfdamage (Bolte et al, 2013).…”