Transcriptomic responses of sponge holobionts to in situ, seasonal anoxia and hypoxia

  1. Brian W. Strehlow
  2. Astrid Schuster
  3. Warren R. Francis
  4. Lisa Eckford-Soper
  5. Beate Kraft
  6. Rob McAllen
  7. Ronni Nielsen
  8. Susanne Mandrup
  9. Donald E. Canfield

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Abstract

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.

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  1. Version published to 10.24072/pcjournal.410
  2. Peer Community In Zoology

    It is now widely accepted that anthropogenic climate change is a severe threat to biodiversity, ecosystem function and associated ecosystem services. Assessing the vulnerability of species and predicting their response to future changes has become a priority for environmental biology (Williams et al. 2020).

    Over the last few decades, oxygen concentrations in both the open ocean and coastal waters have been declining steadily as the result of multiple anthropogenic activities. This global trends towards hypoxia is expected to continue in the future, causing a host of negative effects on marine ecosystems. Oxygen is indeed crucial to many biological processes in the ocean, and its decrease could have strong impacts on biogeochemical cycles, and therefore on marine productivity and biodiversity (Breitburg et al. 2018).

    Whenever facing such drastic environmental changes, all organisms are expected to have some intrinsic ability to adapt. At shorter than evolutionary timescales, ecological plasticity and the eco-physiological processes that sustain it could constitute important adaptive mechanisms (Williams et al. 2020)

    Marine sponges seem particularly well-adapted to oxygen deficiency, as some species can survive seasonal anoxia for several months. This paper by Strehlow et al. (2023) examines the mechanisms allowing this exceptional tolerance. Focusing on two species of sponges, they used transcriptomics to assess how gene expression by sponges, by their mitochondria, or by their unique and species-specific microbiome could facilitate this trait. Their results suggest that sponge holobionts maintain metabolic activity under anoxic conditions while displaying shock response, therefore not supporting the hypothesis of sponge dormancy. Furthermore, hypoxia and anoxia seemed to influence gene expression in different ways, highlighting the complexity of sponge response to deoxygenation. As often, their exciting results raise as many questions as they provide answers and pave the way for more research regarding how anoxia tolerance in marine sponges could give them an advantage in future oceanic environmental conditions.

    References

    Breitburg et al. (2018): Declining oxygen in the global ocean and coastal waters. Science 359, eaam7240. https://doi.org/10.1126/science.aam7240 

    Strehlow et al. (2023): Transcriptomic responses of sponge holobionts to in situ, seasonal anoxia and hypoxia. bioRxiv, 2023.02.27.530229, ver. 4 peer-reviewed and recommended by Peer Community in Zoology.  https://doi.org/10.1101/2023.02.27.530229 

    Williams et al. (2008) Towards an Integrated Framework for Assessing the Vulnerability of Species to Climate Change. PLOS Biology 6(12): e325. https://doi.org/10.1371/journal.pbio.0060325 

    Williams et al. (2020):  Research priorities for natural ecosystems in a changing global climate. Global Change Biology 26: 410–416. https://doi.org/10.1111/gcb.14856 

  3. Version published to 10.1101/2023.02.27.530229 on bioRxiv