The genome of Spironucleus salmonicida highlights a fish pathogen adapted to fluctuating environments

PLoS Genet. 2014 Feb 6;10(2):e1004053. doi: 10.1371/journal.pgen.1004053. eCollection 2014 Feb.

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.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Diplomonadida / genetics*
  • Diplomonadida / pathogenicity
  • Environment
  • Fishes / genetics*
  • Fishes / parasitology
  • Genome*
  • Host-Parasite Interactions / genetics
  • Molecular Sequence Annotation
  • Phylogeny
  • Promoter Regions, Genetic
  • Reactive Oxygen Species
  • Sequence Analysis, DNA*

Substances

  • Reactive Oxygen Species

Grant support

This work was supported by a grant from The Swedish Research Council Formas (www.formas.se; 2010-899). Illumina data was sequenced at SNP SEQ Technology Platform in Uppsala, which is supported by Uppsala University (www.uu.se), Uppsala University Hospital (www.akademiska.se), Science for Life Laboratory (www.scilifelab.se) and the Swedish Research Council (www.vr.se). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.