Abstract
Recent studies have suggested that innate immune responses exhibit characteristics associated with memory linked to modulations in both vertebrates and invertebrates. However, the diverse evolutionary paths taken, particularly within the invertebrate taxa, should lead to similarly diverse innate immunity memory processes. Our understanding of innate immune memory in invertebrates primarily comes from studies of the fruit fly Drosophila melanogaster, the generality of which is unclear. Caenorhabditis elegans typically inhabits soil harboring a variety of fatal microbial pathogens; for this invertebrate, the innate immune system and aversive behavior are the major defensive strategies against microbial infection. However, their characteristics of immunological memory remains infantile. Here we discovered an immunological memory that promoted avoidance and suppressed innate immunity during reinfection with bacteria, which we revealed to be specific to the previously exposed pathogens. During this trade-off switch of avoidance and innate immunity, the chemosensory neurons AWB and ADF modulated production of serotonin and dopamine, which in turn decreased expression of the innate immunity-associated genes and led to enhanced avoidance via the downstream insulin-like pathway. Therefore, our current study profiles the immune memories during C. elegans reinfected by pathogenic bacteria and further reveals that the chemosensory neurons, the neurotransmitter(s), and their associated molecular signaling pathways are responsible for a trade-off switch between the two immunological memories.
Highlights
Immune system of vertebrates produces a faster and increasingly more efficient immune response against the repeated infections because of immunological memory
It has been described that the aversive behavior of C. elegans can be promoted after reinfection by several bacterial pathogens, such as Pseudomonas aeruginosa PA14, Serratia marcescens, or Staphylococcus aureus, whether the immune memory is specific to the pre-exposed pathogen or responds to a broad spectrum of microbes remains to be elucidated
The worms that had been trained by pre-exposure to P. aeruginosa PA14 but were re-exposed to either a Gram-positive pathogen, namely, S. aureus (Fig. 1B, middle panel), or another Gram-negative pathogen, namely, Salmonella typhimurium, did not show avoidance behavior (Fig. 1B, right panel); the avoidance index was fairly low in either naïve or trained worms, and no enhancement of avoidance was observed in each conditioning
Summary
Recent studies have suggested that innate immune responses exhibit characteristics associated with memory linked to modulations in both vertebrates and invertebrates. Caenorhabditis elegans typically inhabits soil harboring a variety of fatal microbial pathogens; for this invertebrate, the innate immune system and aversive behavior are the major defensive strategies against microbial infection. Their characteristics of immunological memory remains infantile. We discovered an immunological memory that promoted avoidance and suppressed innate immunity during reinfection with bacteria, which we revealed to be specific to the previously exposed pathogens. Innate immunity in C. elegans can eliminate the pathogenic microbes that invade the animal’s body, and it has been suggested to involve transforming growth factor b-like, insulin-like (DAF-2/DAF-16), and p38 mitogen-activated protein kinase (MAPK) classical signaling pathways [12]. We reveal a trade-off between these two immunity memories and detail the underlying molecular mechanism
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