Ocean acidification at a coastal CO2 vent induces expression of stress-related transcripts and transposable elements in the sea anemone Anemonia viridis

Abstract

Ocean acidification threatens to disrupt interactions between organisms throughout marine ecosystems. The diversity of reef-building organisms decreases as seawater CO 2 increases along natural gradients, yet soft-bodied animals, such as sea anemones, are often resilient. We sequenced the polyA-enriched transcriptome of adult sea anemone Anemonia viridis and its dinoflagellate symbiont sampled along a natural CO 2 gradient in Italy to assess stress levels in these organisms. We found that about 1.4% of the anemone transcripts, but only ~0.5% of the Symbiodinium sp. transcripts were differentially expressed. Processes enriched at high seawater CO 2 were mainly linked to cellular stress, including significant up-regulation of protective cellular functions and deregulation of metabolic pathways. Transposable elements were differentially expressed at high seawater CO 2 , with an extreme up-regulation (> 100-fold) of the BEL -family of long terminal repeat retrotransposons. Seawater acidified by CO 2 generated a significant stress reaction in A . viridis , but no bleaching was observed and Symbiodinium sp. appeared to be less affected. These observed changes indicate the mechanisms by which A . viridis acclimate to survive chronic exposure to ocean acidification conditions. We conclude that many organisms that are common in acidified conditions may nevertheless incur costs due to hypercapnia and/or lowered carbonate saturation states.

Discovery of novel peptide neurotoxins from sea anemone species

“…At present, high-throughput transcriptomics has been applied to 13 types of sea anemones: Anthopleura elegantissima, Anthopleura dowii, Aiptasia pallida, Anemonia sulcata, Anemonia viridis, Cnidopus japonicus, Exaiptasia pallida, Heteractis crispa, Oulactis sp., Megalactis griffithsi, Nematostella vectensis, Stichodactyla helianthus, and Stichodactyla haddoni [18,46,[130][131][132][133][134][135][136][137][138]. There is a growing body of literature using transcriptomics data to study the symbiotic relationship between sea anemones and their symbionts or to study the mechanism of the evolutionary development of sea anemones [131,139,140].…”

The regulatory role of GABAA receptor in Actinia equina nervous system and the possible effect of global ocean acidification

“…However, how the OA-driven responses alter the behaviour of the soft-bodied forms of anthozoans and modify their long-term ecological perspectives is to a large extent unknown. During the last decade, several research groups have reported a negligible (or even positive) impact of OA on the metabolism of sea anemones of species supporting microalgal endosymbionts of Symbiodinium genus due to rapid changes in endosymbionts’ biochemistry and photosynthesis capacity [ 16 , 20 , 40 ]. Nevertheless, the impact of OA on non-symbiotic sea anemones has yet to be determined.…”

The effects of ocean acidification on the establishment and maintenance of a model cnidarian-dinoflagellate symbiosis

“…Tellingly, anti-apoptotic responses have been reported under decreased pH. Bcl-2 proteins and HSPs, which regulate apoptosis, were upregulated in juvenile A. millepora (Moya et al 2015) and A. viridis (Urbarova et al 2019), suggesting that anti-apoptotic molecules may play an important role in mitigating OA-driven cell loss (Kvitt et al 2011). However, the opposite response was reported by Kaniewska et al (2012) for adult A. millepora, suggesting species-and/or life stage-specific responses, or that longer term exposure to decreased pH may overwhelm these antiapoptotic mechanisms, possibly due to host mitochondrial impairment (Kaniewska et al 2012;Rocker et al 2015;Urbarova et al 2019).…”

“…OA has been shown to increase ROS generation and induce oxidative stress in cnidarians (Luz et al 2018;Urbarova et al 2019). Stress responses may include upregulation of HSPs, molecular chaperones, and glucose-regulated proteins involved in ER stress, UPR and suppression of caspase activation (Kaniewska et al 2012;Moya et al 2015;Urbarova et al 2019). These point to upregulation of host innate immune responses and apoptotic processes under combined OA/OW stress (Kaniewska et al 2015;Urbarova et al 2019).…”

“…Stress responses may include upregulation of HSPs, molecular chaperones, and glucose-regulated proteins involved in ER stress, UPR and suppression of caspase activation (Kaniewska et al 2012;Moya et al 2015;Urbarova et al 2019). These point to upregulation of host innate immune responses and apoptotic processes under combined OA/OW stress (Kaniewska et al 2015;Urbarova et al 2019). Further, expression of phosphoglycolate phosphatase (PGPase), the enzyme that removes phosphoglycolate from symbiont chloroplasts during photorespiration, may be reduced at elevated pCO2 (1160-1500 µatm; Crawley et al 2010).…”