Oxygen induces the expression of invasion and stress response genes in the anaerobic salmon parasite Spironucleus salmonicida
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, s...
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Uppsala universitet, Molekylär evolution
2019
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ftuppsalauniv:oai:DiVA.org:uu-378917 2024-02-11T10:02:13+01:00 Oxygen induces the expression of invasion and stress response genes in the anaerobic salmon parasite Spironucleus salmonicida Stairs, Courtney W. Kokla, Anna Astvaldsson, Asgeir Jerlström-Hultqvist, Jon Svärd, Staffan Ettema, Thijs J. G. 2019 application/pdf http://urn.kb.se/resolve?urn=urn:nbn:se:uu:diva-378917 https://doi.org/10.1186/s12915-019-0634-8 eng eng Uppsala universitet, Molekylär evolution Uppsala universitet, Mikrobiologi Department of Biochemistry and Molecular Biology, Dalhousie University, Halifax, Canada. BMC Biology, 2019, 17:1, orcid:0000-0002-7392-1746 orcid:0000-0002-6898-6377 http://urn.kb.se/resolve?urn=urn:nbn:se:uu:diva-378917 doi:10.1186/s12915-019-0634-8 PMID 30823887 ISI:000459961200001 info:eu-repo/semantics/openAccess Anaerobiosis Diplomonads Giardia Lateral gene transfer Oxygen stress Parasitology Protist RNAseq Spironucleosis Spironucleus Biochemistry and Molecular Biology Biokemi och molekylärbiologi Article in journal info:eu-repo/semantics/article text 2019 ftuppsalauniv https://doi.org/10.1186/s12915-019-0634-8 2024-01-17T23:33:47Z 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 ... Article in Journal/Newspaper Atlantic salmon Uppsala University: Publications (DiVA) BMC Biology 17 1 |
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Open Polar |
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Uppsala University: Publications (DiVA) |
op_collection_id |
ftuppsalauniv |
language |
English |
topic |
Anaerobiosis Diplomonads Giardia Lateral gene transfer Oxygen stress Parasitology Protist RNAseq Spironucleosis Spironucleus Biochemistry and Molecular Biology Biokemi och molekylärbiologi |
spellingShingle |
Anaerobiosis Diplomonads Giardia Lateral gene transfer Oxygen stress Parasitology Protist RNAseq Spironucleosis Spironucleus Biochemistry and Molecular Biology Biokemi och molekylärbiologi Stairs, Courtney W. Kokla, Anna Astvaldsson, Asgeir Jerlström-Hultqvist, Jon Svärd, Staffan Ettema, Thijs J. G. Oxygen induces the expression of invasion and stress response genes in the anaerobic salmon parasite Spironucleus salmonicida |
topic_facet |
Anaerobiosis Diplomonads Giardia Lateral gene transfer Oxygen stress Parasitology Protist RNAseq Spironucleosis Spironucleus Biochemistry and Molecular Biology Biokemi och molekylärbiologi |
description |
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 ... |
format |
Article in Journal/Newspaper |
author |
Stairs, Courtney W. Kokla, Anna Astvaldsson, Asgeir Jerlström-Hultqvist, Jon Svärd, Staffan Ettema, Thijs J. G. |
author_facet |
Stairs, Courtney W. Kokla, Anna Astvaldsson, Asgeir Jerlström-Hultqvist, Jon Svärd, Staffan Ettema, Thijs J. G. |
author_sort |
Stairs, Courtney W. |
title |
Oxygen induces the expression of invasion and stress response genes in the anaerobic salmon parasite Spironucleus salmonicida |
title_short |
Oxygen induces the expression of invasion and stress response genes in the anaerobic salmon parasite Spironucleus salmonicida |
title_full |
Oxygen induces the expression of invasion and stress response genes in the anaerobic salmon parasite Spironucleus salmonicida |
title_fullStr |
Oxygen induces the expression of invasion and stress response genes in the anaerobic salmon parasite Spironucleus salmonicida |
title_full_unstemmed |
Oxygen induces the expression of invasion and stress response genes in the anaerobic salmon parasite Spironucleus salmonicida |
title_sort |
oxygen induces the expression of invasion and stress response genes in the anaerobic salmon parasite spironucleus salmonicida |
publisher |
Uppsala universitet, Molekylär evolution |
publishDate |
2019 |
url |
http://urn.kb.se/resolve?urn=urn:nbn:se:uu:diva-378917 https://doi.org/10.1186/s12915-019-0634-8 |
genre |
Atlantic salmon |
genre_facet |
Atlantic salmon |
op_relation |
BMC Biology, 2019, 17:1, orcid:0000-0002-7392-1746 orcid:0000-0002-6898-6377 http://urn.kb.se/resolve?urn=urn:nbn:se:uu:diva-378917 doi:10.1186/s12915-019-0634-8 PMID 30823887 ISI:000459961200001 |
op_rights |
info:eu-repo/semantics/openAccess |
op_doi |
https://doi.org/10.1186/s12915-019-0634-8 |
container_title |
BMC Biology |
container_volume |
17 |
container_issue |
1 |
_version_ |
1790598150017253376 |