Transcriptomic responses of sponge holobionts to in situ, seasonal anoxia and hypoxia
Deoxygenation can be fatal for many marine animals; however, some sponge species are tolerant of hypoxia and anoxia. Indeed, two sponge species, Eurypon sp. 2 and Hymeraphia stellifera, survive seasonal anoxia for months at a time. To understand their tolerance mechanisms, we performed differential...
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2024-04-01
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| author | Strehlow, Brian W. Schuster, Astrid Francis, Warren R. Eckford-Soper, Lisa Kraft, Beate McAllen, Rob Nielsen, Ronni Mandrup, Susanne Canfield, Donald E. |
| author_facet | Strehlow, Brian W. Schuster, Astrid Francis, Warren R. Eckford-Soper, Lisa Kraft, Beate McAllen, Rob Nielsen, Ronni Mandrup, Susanne Canfield, Donald E. |
| author_sort | Strehlow, Brian W. |
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| description | Deoxygenation can be fatal for many marine animals; however, some sponge species are tolerant of hypoxia and anoxia. Indeed, two sponge species, Eurypon sp. 2 and Hymeraphia stellifera, survive seasonal anoxia for months at a time. To understand their tolerance mechanisms, we performed differential gene expression analyses on the sponges, their mitochondria and their microbial symbionts under in situ conditions of normoxia, hypoxia and anoxia. Each species possessed a unique microbiome, but the microbiomes of each species were dominated by a species-specific Thaumarchaeon and a Gammaproteobacterium. Holobiont gene expression was species-and oxygen-level dependent, though there were some shared interspecific responses to deoxygenation. In general, few changes occurred in the expression of sponge metabolic genes as a function of oxygenation level, indicating that they may remain metabolically active under anoxia. However, ATP synthesis genes were significantly upregulated under hypoxia when compared to normoxia, and genes for DNA replication were downregulated. Mitochondrial gene expression was effectively unchanged under both hypoxia and anoxia. Nevertheless, both anoxia and hypoxia caused upregulation of heat shock proteins (HSPs), indicating cellular level adaptations to deoxygenation stress. A meta-analysis demonstrated that sponge transcriptional responses to anoxia were distinct from those displayed by other invertebrates while dormant, and the hypothesis of sponge dormancy under anoxia was not supported. Thaumarchaeota symbionts also upregulated stress response genes in hypoxia, while maintaining expression of oxygen-dependent metabolic pathways under hypoxia and anoxia. Gammaproteobacteria symbionts showed relatively few noteworthy changes in gene expression in response to anoxia but decreased metabolic gene expression in hypoxia. There was no clear evidence of upregulated anaerobic respiration in the transcriptomes of the sponge holobionts under anoxia or hypoxia. The tolerance of some sponges to prolonged anoxia warrants further investigation and could give them an advantage in future oceans following climate change as well as in ancient oceans when oxygen concentrations were lower than at present. |
| format | Article |
| id | doaj-art-46db9f237b644dd4857e2d08250ba83d |
| institution | Kabale University |
| issn | 2804-3871 |
| language | English |
| publishDate | 2024-04-01 |
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| spelling | doaj-art-46db9f237b644dd4857e2d08250ba83d2025-02-07T10:17:18ZengPeer Community InPeer Community Journal2804-38712024-04-01410.24072/pcjournal.41010.24072/pcjournal.410Transcriptomic responses of sponge holobionts to in situ, seasonal anoxia and hypoxia Strehlow, Brian W.0https://orcid.org/0000-0002-1196-8338Schuster, Astrid1https://orcid.org/0000-0001-8978-3256Francis, Warren R.2https://orcid.org/0000-0003-3473-4726Eckford-Soper, Lisa3https://orcid.org/0000-0003-1118-1962Kraft, Beate4https://orcid.org/0000-0003-0310-5206McAllen, Rob5Nielsen, Ronni6Mandrup, Susanne7https://orcid.org/0000-0002-0961-5787Canfield, Donald E.8Nordcee, Department of Biology, University of Southern Denmark, Odense M, Denmark; Littoral Environnement et Sociétés (LIENSs), UMR 7266 CNRS - La Rochelle Université, 2 Rue Olympe de Gouges, 17000, La Rochelle, FranceNordcee, Department of Biology, University of Southern Denmark, Odense M, DenmarkNordcee, Department of Biology, University of Southern Denmark, Odense M, DenmarkNordcee, Department of Biology, University of Southern Denmark, Odense M, DenmarkNordcee, Department of Biology, University of Southern Denmark, Odense M, DenmarkSchool of Biological, Earth and Environmental Sciences, University College Cork, Cork, IrelandFunctional Genomics and Metabolism Research Unit, Department of Biochemistry and Molecular Biology, University of Southern Denmark, Odense, DenmarkFunctional Genomics and Metabolism Research Unit, Department of Biochemistry and Molecular Biology, University of Southern Denmark, Odense, DenmarkNordcee, Department of Biology, University of Southern Denmark, Odense M, DenmarkDeoxygenation can be fatal for many marine animals; however, some sponge species are tolerant of hypoxia and anoxia. Indeed, two sponge species, Eurypon sp. 2 and Hymeraphia stellifera, survive seasonal anoxia for months at a time. To understand their tolerance mechanisms, we performed differential gene expression analyses on the sponges, their mitochondria and their microbial symbionts under in situ conditions of normoxia, hypoxia and anoxia. Each species possessed a unique microbiome, but the microbiomes of each species were dominated by a species-specific Thaumarchaeon and a Gammaproteobacterium. Holobiont gene expression was species-and oxygen-level dependent, though there were some shared interspecific responses to deoxygenation. In general, few changes occurred in the expression of sponge metabolic genes as a function of oxygenation level, indicating that they may remain metabolically active under anoxia. However, ATP synthesis genes were significantly upregulated under hypoxia when compared to normoxia, and genes for DNA replication were downregulated. Mitochondrial gene expression was effectively unchanged under both hypoxia and anoxia. Nevertheless, both anoxia and hypoxia caused upregulation of heat shock proteins (HSPs), indicating cellular level adaptations to deoxygenation stress. A meta-analysis demonstrated that sponge transcriptional responses to anoxia were distinct from those displayed by other invertebrates while dormant, and the hypothesis of sponge dormancy under anoxia was not supported. Thaumarchaeota symbionts also upregulated stress response genes in hypoxia, while maintaining expression of oxygen-dependent metabolic pathways under hypoxia and anoxia. Gammaproteobacteria symbionts showed relatively few noteworthy changes in gene expression in response to anoxia but decreased metabolic gene expression in hypoxia. There was no clear evidence of upregulated anaerobic respiration in the transcriptomes of the sponge holobionts under anoxia or hypoxia. The tolerance of some sponges to prolonged anoxia warrants further investigation and could give them an advantage in future oceans following climate change as well as in ancient oceans when oxygen concentrations were lower than at present.https://peercommunityjournal.org/articles/10.24072/pcjournal.410/Sponges, deoxygenation, microbiome, gene expression, marine, Thaumarchaeota, Gammaproteobacteria |
| spellingShingle | Strehlow, Brian W. Schuster, Astrid Francis, Warren R. Eckford-Soper, Lisa Kraft, Beate McAllen, Rob Nielsen, Ronni Mandrup, Susanne Canfield, Donald E. Transcriptomic responses of sponge holobionts to in situ, seasonal anoxia and hypoxia Peer Community Journal Sponges, deoxygenation, microbiome, gene expression, marine, Thaumarchaeota, Gammaproteobacteria |
| title | Transcriptomic responses of sponge holobionts to in situ, seasonal anoxia and hypoxia
|
| title_full | Transcriptomic responses of sponge holobionts to in situ, seasonal anoxia and hypoxia
|
| title_fullStr | Transcriptomic responses of sponge holobionts to in situ, seasonal anoxia and hypoxia
|
| title_full_unstemmed | Transcriptomic responses of sponge holobionts to in situ, seasonal anoxia and hypoxia
|
| title_short | Transcriptomic responses of sponge holobionts to in situ, seasonal anoxia and hypoxia
|
| title_sort | transcriptomic responses of sponge holobionts to in situ seasonal anoxia and hypoxia |
| topic | Sponges, deoxygenation, microbiome, gene expression, marine, Thaumarchaeota, Gammaproteobacteria |
| url | https://peercommunityjournal.org/articles/10.24072/pcjournal.410/ |
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