Abstract
BackgroundSpironucleus salmonicida is an anaerobic parasite that can cause systemic infections in Atlantic salmon. Unlike other diplomonad parasites, such as the human pathogen Giardia intestinalis, Spironucleus species can infiltrate the blood stream of their hosts eventually colonizing organs, skin and gills. How this presumed anaerobe can persist and invade oxygenated tissues, despite having a strictly anaerobic metabolism, remains elusive.ResultsTo investigate how S. salmonicida response to oxygen stress, we performed RNAseq transcriptomic analyses of cells grown in the presence of oxygen or antioxidant-free medium. We found that over 20% of the transcriptome is differentially regulated in oxygen (1705 genes) and antioxidant-depleted (2280 genes) conditions. 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. salmonicida does not encode genes involved in the classical elements of oxygen metabolism (e.g., catalases, superoxide dismutase, glutathione biosynthesis, oxidative phosphorylation). Instead, we found that genes encoding bacterial-like oxidoreductases were upregulated in response to oxygen stress. Phylogenetic analysis revealed some of these oxygen-responsive genes (e.g., nadh oxidase, rubrerythrin, superoxide reductase) are rare in eukaryotes and likely derived from lateral gene transfer (LGT) events into diplomonads from prokaryotes. Unexpectedly, we observed that many host evasion- and invasion-related genes were also upregulated under oxidative stress suggesting that oxygen might be an important signal for pathogenesis.ConclusionWhile oxygen is toxic for related organisms, such as G. intestinalis, we find that oxygen is likely a gene induction signal for host invasion- and evasion-related pathways in S. salmonicida. These data provide the first molecular evidence for how S. salmonicida could tolerate oxic host environments and demonstrate how LGT can have a profound impact on the biology of anaerobic parasites.
Highlights
Spironucleus salmonicida is an anaerobic parasite that can cause systemic infections in Atlantic salmon
To investigate how S. salmonicida responds to oxygen and oxidative stress, cells were exposed to oxygen (OXY) or maintained in medium lacking antioxidants (NAO) (Fig. 1a, b)
We propose that S. salmonicida uses a system that uses RBR, Superoxide reductase (SOR), and Flavodiiron protein (FDP) together with flavodoxin-related proteins (FLD) and an FLD oxidoreductase such as Pyruvate: ferredoxin oxidoreductase (PFO); similar systems have been proposed in bacteria [85]
Summary
Spironucleus salmonicida is an anaerobic parasite that can cause systemic infections in Atlantic salmon. Unlike other diplomonad parasites, such as the human pathogen Giardia intestinalis, Spironucleus species can infiltrate the blood stream of their hosts eventually colonizing organs, skin and gills. How this presumed anaerobe can persist and invade oxygenated tissues, despite having a strictly anaerobic metabolism, remains elusive. The life cycle comprises two main stages: the trophozoite, the actively replicating symptomatic stage, and the cyst, the environmentally resistant infective stage shed in host stools [2, 3] Another lineage of parasitic diplomonads includes Spironucleus species known to infect a wide array of animals including birds, primates, and mice [4,5,6]. Advancing our current understanding of this parasite’s biology is essential for developing alternative treatment strategies and to block transmission cycles
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