Resilience to ocean acidification: decreased carbonic anhydrase activity in sea anemones under high pCO2 conditions

Ventura, Patrícia; Jarrold, Michael D.; Merle, Pierre Laurent; Barnay‐Verdier, Stéphanie; Zamoum, Thamilla; Rodolfo‐Metalpa, Riccardo; Calosi, Piero; Furla, Paola

doi:10.3354/meps11916

Cited by 20 publications

(17 citation statements)

References 28 publications

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“…Indeed, any increase in net oxygen production must equate to a net increase in CO 2 fixation during photosynthesis (Reece et al, 2015). In addition to reduced costs of carbon acquisition under high pCO 2 (Ventura et al, 2016), we hypothesize that inhibition of photorespiration may also partially explain the higher rate of asexual reproduction of symbiotic polyps under acidification alone due to increased efficiency of carbon fixation and increased availability of organic carbon for growth. Clearly, better understanding processes such as photorespiration is needed to assess why only some Symbiodinium types, that is perhaps those more susceptible to…”

Section: Discussionmentioning

confidence: 97%

“…Elevated p CO 2 of surrounding seawater may also stimulate the photosynthetic activity of Symbiodinium spp. where cells have become CO 2 limited (see Gibbin et al., ; Suggett et al., , ; Ventura et al., ) and may act as a key condition needed to enhance oxygenation of the host tissues. Whilst this potential mitigating role of endosymbiotic algae is interesting, it may ultimately be restricted to certain Symbiodinium spp.…”

Section: Introductionmentioning

confidence: 99%

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Symbiodinium mitigate the combined effects of hypoxia and acidification on a noncalcifying cnidarian

Klein

Pitt

Nitschke

et al. 2017

Global Change Biology

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Anthropogenic nutrient inputs enhance microbial respiration within many coastal ecosystems, driving concurrent hypoxia and acidification. During photosynthesis, Symbiodinium spp., the microalgal endosymbionts of cnidarians and other marine phyla, produce O and assimilate CO and thus potentially mitigate the exposure of the host to these stresses. However, such a role for Symbiodinium remains untested for noncalcifying cnidarians. We therefore contrasted the fitness of symbiotic and aposymbiotic polyps of a model host jellyfish (Cassiopea sp.) under reduced O (~2.09 mg/L) and pH (~ 7.63) scenarios in a full-factorial experiment. Host fitness was characterized as asexual reproduction and their ability to regulate internal pH and Symbiodinium performance characterized by maximum photochemical efficiency, chla content and cell density. Acidification alone resulted in 58% more asexual reproduction of symbiotic polyps than aposymbiotic polyps (and enhanced Symbiodinium cell density) suggesting Cassiopea sp. fitness was enhanced by CO -stimulated Symbiodinium photosynthetic activity. Indeed, greater CO drawdown (elevated pH) was observed within host tissues of symbiotic polyps under acidification regardless of O conditions. Hypoxia alone produced 22% fewer polyps than ambient conditions regardless of acidification and symbiont status, suggesting Symbiodinium photosynthetic activity did not mitigate its effects. Combined hypoxia and acidification, however, produced similar numbers of symbiotic polyps compared with aposymbiotic kept under ambient conditions, demonstrating that the presence of Symbiodinium was key for mitigating the combined effects of hypoxia and acidification on asexual reproduction. We hypothesize that this mitigation occurred because of reduced photorespiration under elevated CO conditions where increased net O production ameliorates oxygen debt. We show that Symbiodinium play an important role in facilitating enhanced fitness of Cassiopea sp. polyps, and perhaps also other noncalcifying cnidarian hosts, to the ubiquitous effects of ocean acidification. Importantly we highlight that symbiotic, noncalcifying cnidarians may be particularly advantaged in productive coastal waters that are subject to simultaneous hypoxia and acidification.

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Section: Discussionmentioning

confidence: 97%

Section: Introductionmentioning

confidence: 99%

Symbiodinium mitigate the combined effects of hypoxia and acidification on a noncalcifying cnidarian

Klein

Pitt

Nitschke

et al. 2017

Global Change Biology

View full text Add to dashboard Cite

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“…A second protein of interest is a membrane-bound and excreted enzyme in the carbonic anhydrase family (SPU_012518). Carbonic anhydrases catalyse the hydration of CO 2 to bicarbonate [66] and have been shown to be responsive to experimental acidification in many organisms, including purple sea urchin [27,56], corals [67], anemones [68], mussels [69], oysters [70] and giant kelp [71]. In the royalsocietypublishing.org/journal/rspb Proc.…”

Section: (C) Mechanisms For Response To Low-ph Conditionsmentioning

confidence: 99%

Rare genetic variation and balanced polymorphisms are important for survival in global change conditions

et al. 2019

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Standing genetic variation is important for population persistence in extreme environmental conditions. While some species may have the capacity to adapt to predicted average future global change conditions, the ability to survive extreme events is largely unknown. We used single-generation selection experiments on hundreds of thousands of Strongylocentrotus purpuratus sea urchin larvae generated from wild-caught adults to identify adaptive genetic variation responsive to moderate (pH 8.0) and extreme (pH 7.5) low-pH conditions. Sequencing genomic DNA from pools of larvae, we identified consistent changes in allele frequencies across replicate cultures for each pH condition and observed increased linkage disequilibrium around selected loci, revealing selection on recombined standing genetic variation. We found that loci responding uniquely to either selection regime were at low starting allele frequencies while variants that responded to both pH conditions (11.6% of selected variants) started at high frequencies. Loci under selection performed functions related to energetics, pH tolerance, cell growth and actin/cytoskeleton dynamics. These results highlight that persistence in future conditions will require two classes of genetic variation: common, pH-responsive variants maintained by balancing selection in a heterogeneous environment, and rare variants, particularly for extreme conditions, that must be maintained by large population sizes.

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“…Moreover, previous studies investigating the nature of A. viridis morphs did not systematically consider A. viridis as a holobiont. A. viridis' gastrodermal tissue harbours millions of dinoଏagellate cells (Muscatine et al 1998;Suggett et al 2012;Zamoum and Furla 2012;Ventura et al 2016) belonging to the family Symbiodiniaceae (LaJeunesse et al 2018) that live in a close trophic relationship (Davy et al 1996) and that are vertically transmitted (Schäfer 1984). The Symbiodiniaceae associated to A. viridis belong to the temperate clade A (LaJeunesse et al 2018; or A' sensu Savage et al 2002;Visram et al 2006) presenting not only an intra-clade genetic diversity partially structured by host species but also an intra-host genetic diversity (Visram et al 2006;Forcioli et al 2011;Casado-Amezúa et al 2014).…”

Section: Introductionmentioning

confidence: 99%

The many faced symbiotic snakelocks anemone (Anemonia viridis, Anthozoa): host and symbiont genetic differentiation among colour morphs

et al. 2019

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How can we explain morphological variations in a holobiont? The genetic determinism of phenotypes is not always obvious and could be circumstantial in complex organisms. In symbiotic cnidarians, it is known that morphology or colour can misrepresent a complex genetic and symbiotic diversity. Anemonia viridis is a symbiotic sea anemone from temperate seas. This species displays different colour morphs based on pigment content and lives in a wide geographical range. Here, we investigated whether colour morph differentiation correlated with host genetic diversity or associated symbiotic genetic diversity by using RAD sequencing and symbiotic dinoଏagellate typing of 140 sea anemones from the English Channel and the Mediterranean Sea. We did not observe genetic differentiation among colour morphs of A. viridis at the animal host or symbiont level, rejecting the hypothesis that A. viridis colour morphs correspond to species level differences. Interestingly, we however identiଏed at least four independent animal host genetic lineages in A. viridis that differed in their associated symbiont populations. In conclusion, although the functional role of the different morphotypes of A. viridis remains to be determined, our approach provides new insights on the existence of cryptic species within A. viridis.

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Resilience to ocean acidification: decreased carbonic anhydrase activity in sea anemones under high pCO2 conditions

Cited by 20 publications

References 28 publications

Symbiodinium mitigate the combined effects of hypoxia and acidification on a noncalcifying cnidarian

Symbiodinium mitigate the combined effects of hypoxia and acidification on a noncalcifying cnidarian

Rare genetic variation and balanced polymorphisms are important for survival in global change conditions

The many faced symbiotic snakelocks anemone (Anemonia viridis, Anthozoa): host and symbiont genetic differentiation among colour morphs

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