The Genome of Spironucleus salmonicida Highlights a Fish Pathogen Adapted to Fluctuating Environments

Abstract

Spironucleus salmonicida causes systemic infections in salmonid fish. It belongs to the group diplomonads, binucleated heterotrophic flagellates adapted to micro-aerobic environments. Recently we identified energy-producing hydrogenosomes in S. salmonicida. Here we present a genome analysis of the fish parasite with a focus on the comparison to the more studied diplomonad Giardia intestinalis. We annotated 8067 protein coding genes in the ∼12.9 Mbp S. salmonicida genome. Unlike G. intestinalis, promoter-like motifs were found upstream of genes which are correlated with gene expression, suggesting a more elaborate transcriptional regulation. S. salmonicida can utilise more carbohydrates as energy sources, has an extended amino acid and sulfur metabolism, and more enzymes involved in scavenging of reactive oxygen species compared to G. intestinalis. Both genomes have large families of cysteine-rich membrane proteins. A cluster analysis indicated large divergence of these families in the two diplomonads. Nevertheless, one of S. salmonicida cysteine-rich proteins was localised to the plasma membrane similar to G. intestinalis variant-surface proteins. We identified S. salmonicida homologs to cyst wall proteins and showed that one of these is functional when expressed in Giardia. This suggests that the fish parasite is transmitted as a cyst between hosts. The extended metabolic repertoire and more extensive gene regulation compared to G. intestinalis suggest that the fish parasite is more adapted to cope with environmental fluctuations. Our genome analyses indicate that S. salmonicida is a well-adapted pathogen that can colonize different sites in the host.

Identification of Obscure yet Conserved Actin-Associated Proteins in Giardia lamblia

“…The genome of Spironucleus salmonicida, another diplomonad and close relative of Giardia, was recently released (33). As part of our analysis, we compared our list of putative actin interactors to the S. salmonicida genome (Table 1) (33).…”

“…As part of our analysis, we compared our list of putative actin interactors to the S. salmonicida genome (Table 1) (33). Although most of the identified proteins are present in S. salmonicida, several appear to be specific to Giardia.…”

Probing the Biology of Giardia intestinalis Mitosomes Using In Vivo Enzymatic Tagging

“…Surprisingly, no Tim44 ortholog was identified in the recently published genome of the hydrogenosome-bearing fish parasite S. salmonicida (45). According to further HMM-based searches, Tim44 has been lost several times in the evolution of eukaryotes.…”

Diversity and origins of anaerobic metabolism in mitochondria and related organelles

“…Like Trichomonas, Giardia also synthesizes ATP by the arginine dihydrolase pathway; however, this pathway is entirely cytosolic in this organism [32]. The MROs of Spironucleus salmonicida, a related diplomonad parasite of salmonid fish [33,34], resemble Trichomonas hydrogenosomes in possessing a hydrogen-producing extended glycolysis pathway, Fe-S cluster generation, and possibly glycine metabolism. ATP is produced in these organelles by the Giardia-like ACS system, and not the ASCT/SCS system seen in Trichomonas [33,34].…”

“…The MROs of Spironucleus salmonicida, a related diplomonad parasite of salmonid fish [33,34], resemble Trichomonas hydrogenosomes in possessing a hydrogen-producing extended glycolysis pathway, Fe-S cluster generation, and possibly glycine metabolism. ATP is produced in these organelles by the Giardia-like ACS system, and not the ASCT/SCS system seen in Trichomonas [33,34]. Putative MROs have been described in many different species of the flagellated metamonad genus Trimastix [35][36][37][38].…”