Abstract
BackgroundImmune responses need to be initiated rapidly, and maintained as needed, to prevent establishment and growth of infections. At the same time, resources need to be balanced with other physiological processes. On the level of transcription, studies have shown that this balancing act is reflected in tight control of the initiation kinetics and shutdown dynamics of specific immune genes.ResultsTo investigate genome-wide expression dynamics and trade-offs after infection at a high temporal resolution, we performed an RNA-seq time course on D. melanogaster with 20 time points post Imd stimulation. A combination of methods, including spline fitting, cluster analysis, and Granger causality inference, allowed detailed dissection of expression profiles, lead-lag interactions, and functional annotation of genes through guilt-by-association. We identified Imd-responsive genes and co-expressed, less well characterized genes, with an immediate-early response and sustained up-regulation up to 5 days after stimulation. In contrast, stress response and Toll-responsive genes, among which were Bomanins, demonstrated early and transient responses. We further observed a strong trade-off with metabolic genes, which strikingly recovered to pre-infection levels before the immune response was fully resolved.ConclusionsThis high-dimensional dataset enabled the comprehensive study of immune response dynamics through the parallel application of multiple temporal data analysis methods. The well annotated data set should also serve as a useful resource for further investigation of the D. melanogaster innate immune response, and for the development of methods for analysis of a post-stress transcriptional response time-series at whole-genome scale.
Highlights
Immune responses need to be initiated rapidly, and maintained as needed, to prevent establishment and growth of infections
Immune responses are energetically costly [1] because they draw resources from other physiological processes [2, 3] such as metabolism, reproduction, and environmental stress responses
We found that commercial LPS exposure has a major impact on the expression of immune genes, and genes involved in metabolism and replication stress
Summary
Immune responses need to be initiated rapidly, and maintained as needed, to prevent establishment and growth of infections. We expect that natural selection will act to tune the immune response to strike a balance between the advantage of a rapid and Schlamp et al BMC Genomics (2021) 22:304 robust ability to fight infection, and the costly sideeffects of an over-prolonged immune response. This tuning is likely to be mediated through a series of regulatory and feedback properties of the immune system of the fly
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