Friend or foe? Effects of host immune activation on the transient gut microbiome in the caterpillar Manduca sexta

Abstract

For many animals the gut microbiome plays an essential role in immunity and digestion. However, certain animals, such as the caterpillar Manduca sexta, do not have a resident gut microbiome. Although these animals do have bacteria that pass through their gut from their natural environment, the absence of such bacteria does not reduce growth or survival. We hypothesized that Manduca sexta would sterilize their gut as a protective measure against secondary infection when faced with a gut infection, or exposure to heat-killed bacteria in the blood (hemolymph). However, we found that gut sterilization did not occur during either type of immune challenge, i.e. bacterial numbers did not decrease. By examing the pattern of immune-related gene expression, gut pH, live bacterial counts, and weight change (as a measure of sickness behaviour), we found evidence for physiological trade-offs between between regulating the microbiome and defending against systemic infections. Caterpillars exposed to both gut pathogens and a systemic immune challenge had higher numbers of bacteria in their gut than caterpillars exposed to a single challenge. Following a principal component analysis, we found that the response patterns following an oral challenge, systemic challenge or dual challenge were unique. Our results suggest that the immune response for each challenge resulted in a different configuration of the immunophysiological network. We hypothesize that these different configurations represent different resolutions of physiological trade-offs based on the immune responses needed to best protect against the present immune challenges. SUMMARY STATEMENTThis paper investigates the strategies that animals may use to regulate their microbiome during infection.