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Oxygen induces the expression of invasion and stress response genes in the anaerobic salmon parasite Spironucleus salmonicida

Stairs, Courtney W. LU orcid ; Kokla, Anna ; Ástvaldsson, Ásgeir ; Jerlström-Hultqvist, Jon ; Svärd, Staffan and Ettema, Thijs J.G. (2019) In BMC Biology 17.
Abstract

Background: 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. Results: To 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... (More)

Background: 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. Results: To 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. Conclusion: While 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.

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author
; ; ; ; and
publishing date
type
Contribution to journal
publication status
published
keywords
Anaerobiosis, Diplomonads, Giardia, Lateral gene transfer, Oxygen stress, Parasitology, Protist, RNAseq, Spironucleosis, Spironucleus
in
BMC Biology
volume
17
article number
19
pages
21 pages
publisher
BioMed Central (BMC)
external identifiers
  • pmid:30823887
  • scopus:85062413936
ISSN
1741-7007
DOI
10.1186/s12915-019-0634-8
language
English
LU publication?
no
id
c7d98be7-7894-4f14-bfcc-6ffc7223a747
date added to LUP
2020-10-23 10:53:38
date last changed
2024-05-01 18:44:59
@article{c7d98be7-7894-4f14-bfcc-6ffc7223a747,
  abstract     = {{<p>Background: 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. Results: To 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. Conclusion: While 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.</p>}},
  author       = {{Stairs, Courtney W. and Kokla, Anna and Ástvaldsson, Ásgeir and Jerlström-Hultqvist, Jon and Svärd, Staffan and Ettema, Thijs J.G.}},
  issn         = {{1741-7007}},
  keywords     = {{Anaerobiosis; Diplomonads; Giardia; Lateral gene transfer; Oxygen stress; Parasitology; Protist; RNAseq; Spironucleosis; Spironucleus}},
  language     = {{eng}},
  month        = {{03}},
  publisher    = {{BioMed Central (BMC)}},
  series       = {{BMC Biology}},
  title        = {{Oxygen induces the expression of invasion and stress response genes in the anaerobic salmon parasite Spironucleus salmonicida}},
  url          = {{http://dx.doi.org/10.1186/s12915-019-0634-8}},
  doi          = {{10.1186/s12915-019-0634-8}},
  volume       = {{17}},
  year         = {{2019}},
}