Oxygen induces the expression of invasion and stress response genes in the anaerobic salmon parasite Spironucleus salmonicida
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 o...
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| Format: | Article |
| Language: | English |
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BMC
2019-03-01
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| Series: | BMC Biology |
| Subjects: | |
| Online Access: | http://link.springer.com/article/10.1186/s12915-019-0634-8 |
| _version_ | 1818493815227416576 |
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| author | Courtney W. Stairs Anna Kokla Ásgeir Ástvaldsson Jon Jerlström-Hultqvist Staffan Svärd Thijs J. G. Ettema |
| author_facet | Courtney W. Stairs Anna Kokla Ásgeir Ástvaldsson Jon Jerlström-Hultqvist Staffan Svärd Thijs J. G. Ettema |
| author_sort | Courtney W. Stairs |
| collection | DOAJ |
| description | 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 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. |
| first_indexed | 2024-12-10T17:58:51Z |
| format | Article |
| id | doaj.art-dcf59558722148e28d8c7deb8f815e22 |
| institution | Directory Open Access Journal |
| issn | 1741-7007 |
| language | English |
| last_indexed | 2024-12-10T17:58:51Z |
| publishDate | 2019-03-01 |
| publisher | BMC |
| record_format | Article |
| series | BMC Biology |
| spelling | doaj.art-dcf59558722148e28d8c7deb8f815e222022-12-22T01:38:52ZengBMCBMC Biology1741-70072019-03-0117112110.1186/s12915-019-0634-8Oxygen induces the expression of invasion and stress response genes in the anaerobic salmon parasite Spironucleus salmonicidaCourtney W. Stairs0Anna Kokla1Ásgeir Ástvaldsson2Jon Jerlström-Hultqvist3Staffan Svärd4Thijs J. G. Ettema5Department of Cell and Molecular Biology, Uppsala UniversityPresent Address: Department of Plant Biology, Swedish University of Agricultural Sciences (SLU)Department of Cell and Molecular Biology, Uppsala UniversityPresent Address: Department of Biochemistry and Molecular Biology, Dalhousie UniversityDepartment of Cell and Molecular Biology, Uppsala UniversityDepartment of Cell and Molecular Biology, Uppsala UniversityAbstract 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.http://link.springer.com/article/10.1186/s12915-019-0634-8SpironucleusDiplomonadsGiardiaOxygen stressRNAseqAnaerobiosis |
| spellingShingle | Courtney W. Stairs Anna Kokla Ásgeir Ástvaldsson Jon Jerlström-Hultqvist Staffan Svärd Thijs J. G. Ettema Oxygen induces the expression of invasion and stress response genes in the anaerobic salmon parasite Spironucleus salmonicida BMC Biology Spironucleus Diplomonads Giardia Oxygen stress RNAseq Anaerobiosis |
| title | 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_short | 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 |
| topic | Spironucleus Diplomonads Giardia Oxygen stress RNAseq Anaerobiosis |
| url | http://link.springer.com/article/10.1186/s12915-019-0634-8 |
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