Differential expression analysis of Spironucleus salmonicida in response to oxygen stress

Abstract

Background: Spironucleus salmonicida is an anaerobic diplomonad parasite that can cause systemic infections in multiple species of fish including Atlantic salmon. Unlike other anaerobic or microaerophilic gut parasites, such as its close relative Giardia intestinalis, S. salmonicida is able to leave the animal gut via the blood stream eventually colonizing organs, skin and gills, although the precise life cycle and transmissive (i.e., cyst) form of this parasite has not been determined. How this presumed anaerobe can persist and invade oxygenated tissues despite having a strictly anaerobic metabolism remains elusive. Results: To investigate gene expression-level changes specifically related to oxygen stress and tolerance in S. salmoncida, we performed RNAseq transcriptomic analyses of cells grown in presence of oxygen or in media depleted of antioxidants. We found that over 20% of the transcriptome is differentially regulated in both oxygen (1705 genes) and antioxidant-depleted conditions (2280 genes). These differentially regulated transcripts encode proteins related to anaerobic metabolism, cysteine and Fe-S cluster biosynthesis, as well as, a large number of proteins of unknown function. S. salmoncida does not encode genes involved in the classical elements of oxygen-defense (e.g. catalases, superoxide dismutase, glutathione biosynthesis). Instead, we identified a vast repertoire of bacterial-like oxidoreductases likely acquired by lateral gene transfer (LGT) that are upregulated in response to oxygen and anti-oxidant depletion, suggesting that the acquisition of these proteins has been critical for oxygen adaptation of this parasite. Unexpectedly, we observed that many invasion-related genes were upregulated under oxidative stress suggesting that oxygen might be a signal for pathogenesis. Conclusion: These data provide the first molecular evidence for how S. salmonicida is able to and tolerate different oxygen tensions to ultimately colonize different host environments. While oxygen is toxic for other metamonad parasites, such as Giardia, we find that oxygen is actually an gene induction signal for many host invasion and evasion-related pathways