Impact of Ocean Warming and Acidification on Symbiosis Establishment and Gene Expression Profiles in Recruits of Reef Coral Acropora intermedia

Sun, Yuhan; Jiang, Lei; Gong, Sanqiang; Guo, Ming; Yuan, Xiangcheng; Zhou, Guowei; Lei, Xinming; Zhang, Yuyang; Yuan, Tao; Ji, Lian; Qian, Pei‐Yuan; Huang, Hui

doi:10.3389/fmicb.2020.532447

Cited by 15 publications

(16 citation statements)

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“…These results suggest the complex role of larval aggregation in shaping post-settlement performance of corals in response to ocean warming and acidification, and provide direct evidence for the benefits and tradeoff associated with coral chimerism in determining the recruitment success under future climate change. Uptake of algal symbionts and symbiosis establishment are of paramount importance to the early success and resilience of broadcast spawning corals (Suzuki et al, 2013;Yuyama and Higuchi, 2014;Hazraty-Kari et al, 2022), while this process is particularly susceptible to the ongoing ocean warming (Abrego et al, 2012;Yuyama et al, 2016;Yorifuji et al, 2017;Sun et al, 2020;Jiang et al, 2021;Williamson et al, 2021). Consistent with these aforementioned studies, our results also showed detrimental effects of heat stress on symbiont infection process, with symbiont infection rates being reduced by 50% at 30.5°C.…”

Section: Discussionsupporting

confidence: 89%

“…Similarly, Suwa et al (2010) observed that elevated pCO 2 delayed symbiont acquisition in primary polyps of A. digitifera. Nevertheless, two prior studies also reported negligible effects of high pCO 2 on symbiont uptake in recruits of the reef coral A. intermedia and Platygyra daedalea (Sun et al, 2020;Jiang et al, 2021). Therefore, this disparity suggests that the responses of symbiont acquisition in coral recruits to ocean acidification may be highly species-specific.…”

Section: Discussionmentioning

confidence: 89%

“…Coral recruits are of vast importance to maintain adult populations and aid reef recovery, while they are extremely vulnerable and subject to high mortality rates (Ritson-Williams et al, 2009;Harrison, 2011), and this situation may be further compounded by the ongoing ocean warming and acidification driven by climate change (Anlauf et al, 2011;Foster et al, 2015;Jiang et al, 2018;Sun et al, 2020;Jiang et al, 2021). Despite the widely-accepted advantages and benefits with regard to coral chimerism, few studies have directly addressed the ecological consequences of coral chimerism in these susceptible early life history stages under future oceanic conditions.…”

Section: Introductionmentioning

confidence: 99%

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Gregarious larval settlement mediates the responses of new recruits of the reef coral Acropora austera to ocean warming and acidification

Jiang

Zhang²,

Liu³

et al. 2022

Front. Mar. Sci.

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Gregarious larval settlement represents an important window for chimera formation in reef corals, yet it remains largely unknown how aggregated settlement and early chimerism could modify the performance and responses of coral recruits under elevated temperature and pCO2. In this study, single and aggregated recruits of the broadcast spawning coral Acropora austera were exposed to contrasts of two temperatures (28 versus 30.5°C) and pCO2 levels (~500 versus 1000 μatm) for two weeks, and algal symbiont infection success, survivorship and growth were assessed. Results showed that symbiont infection success was mainly affected by temperature and recruit type, with reduced symbiont infection at increased temperature and consistently higher infection success in chimeric recruits compared to single recruits. Furthermore, although chimeric recruits with larger areal size had significantly higher survivorship in all treatments, the polyp-specific growth rates were considerably lower in chimeric entities than individual recruits. More importantly, the recruit type significantly influenced the responses of recruit polyp-specific growth rates to elevated temperature, with chimeras exhibiting lowered skeletal lateral growth under elevated temperature. These results demonstrate the benefits and costs associated with gregarious larval settlement for juvenile corals under ocean warming and acidification, and highlight the ecological role of larval settlement behavior in mediating the responses of coral recruits to climate change stressors.

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Section: Discussionsupporting

confidence: 89%

Section: Discussionmentioning

confidence: 89%

Section: Introductionmentioning

confidence: 99%

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Gregarious larval settlement mediates the responses of new recruits of the reef coral Acropora austera to ocean warming and acidification

Jiang

Zhang²,

Liu³

et al. 2022

Front. Mar. Sci.

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“…Compared to adult corals, early life-history stages generally have more diverse endosymbiont communities (Quigley et al, 2017), which eventually winnow to a more stable, lower diversity community (Lee et al, 2016, Rouzé et al, 2019. In some cases, symbiont communities in juvenile corals may be impacted by environmental factors such as increased temperature and light (Abrego et al, 2012), pCO2 (Suwa et al, 2010) or completely halted by increased temperatures with minimal impacts of pCO2 (Sun et al, 2020). Moreover, the acquisition of symbionts during coral early life-history stages has been assessed only for a limited number of coral species (Cantin et al, 2009, Yorifuji et al, 2017, Quigley et al, 2019, Quigley et al, 2020, and the effects of elevated temperature and pCO2 on this process are poorly understood.…”

Section: Introductionmentioning

confidence: 99%

The promotion of stress tolerant Symbiodiniaceae dominance in juveniles of two coral species due to simulated future conditions of ocean warming and acidification

Terrell

Marangon

Webster

et al. 2021

Preprint

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SummaryThe symbiotic relationship between coral and its endosymbiotic algae, Symbiodiniaceae, greatly influences the hosts’ potential to withstand environmental stress. To date, the effects of climate change on this relationship has primarily focused on adult corals. Uncovering the effects of environmental stress on the establishment and development of this symbiosis in early life stages is critical for predicting how corals may respond to climate change. To determine the impacts of future climate projections on the establishment of symbionts in juvenile corals, ITS2 amplicon sequencing of single coral juveniles was applied to Goniastrea retiformis and Acropora millepora before and after exposure to three climate conditions of varying temperature and pCO2 levels (current and RCP8.5 in 2050 and 2100). Compared to ambient conditions, juvenile corals experienced shuffling in the relative abundance of Cladocopium (C1m, reduction) to Durusdinium (D1 and D1a, increase) over time. We calculated a novel risk metric incorporating functional redundancy and likelihood of impact on host physiology to identify the loss of D1a as a ‘low risk’ to the coral compared to the loss of “higher risk” taxa like D1 and C1m. Although the increase in stress tolerant Durusdinium under future warming was encouraging for A. millepora, by 2100, G. retiformis communities displayed signs of symbiosis de-regulation, suggesting this acclimatory mechanism may have species-specific thresholds. These results emphasize the need for understanding of long-term effects of climate change induced stress on coral juveniles and their potential for increased acclimation to heat tolerance through changes in symbiosis.Originality StatementHere we assessed changes in the uptake and establishment of Symbiodiniaceae in the early lifehistory stages of two coral species under future climate scenarios. Our study represents the first such assessment of future climate change projections (increased temperature and pCO2) influencing Symbiodiniaceae acquisition and specifically shows a community structure dominated by the stress tolerant genus Durusdinium. We also develop a novel risk metric that includes taxonomic function and redundancy to estimate the impact of symbiont taxa changes on coral physiology. Through the risk metric, we relate the stress-induced changes in symbiont community structure to the likelihood of functional loss to better understand the extent to which these changes may lead to a decrease in coral health.

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“…Moreover, very few studies have explored the effects of OA on the establishment phase of the cnidarian-dinoflagellate symbiosis, and these provide a mixed picture. For example, some report no discernible effect of OA (Sun et al 2020;Jiang et al 2021), while others report delayed colonisation (Suwa et al 2010) or reduced symbiosis establishment success (Noonan et al 2013). More is known about the effects of OA on maintenance of the symbiosis, including changes in photosynthesis and respiration (Suggett et al 2012;Towanda and Thuesen 2012;Strahl et al 2016;Biscere et al 2019), symbiont density (Anthony et al 2008;Krief et al 2010;Jarrold et al 2013;Tremblay et al 2013;Ventura et al 2016;Klein et al 2017;Mason 2018) and cellular homeostasis (Kaniewska et al 2012;; however reports are often contradictory across species.…”

Section: Aims and Objectivesmentioning

confidence: 99%

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

Bown¹

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Coral reefs are increasingly under threat from the effects of anthropogenic climate change, including rising sea surface temperatures and more acidified waters. At the foundation of these diverse and valuable ecosystems is the symbiotic relationship between calcifying corals and their endosymbiotic dinoflagellate algae, Symbiodiniaceae – one that is particularly sensitive to environmental stressors. Ocean acidification (OA) results in the lowering of pH and changes to carbonate chemistry and the inorganic carbon species available to marine organisms. Cnidarians such as reef-building corals may be particularly at risk from OA, as changes in pH and carbon availability can alter central physiological processes, including calcification, photosynthesis, acid-base regulation, metabolism and cell-cycle regulation. Yet, while responses to OA have been well researched at the physiological level, results have often been contradictory, and a clear understanding of the nature and extent of impacts on the cnidarian-dinoflagellate symbiosis remains equivocal. This thesis therefore aimed to provide further insights into the effects of OA on the establishment and maintenance of the cnidarian-dinoflagellate symbiosis. My research utilised the well-established model system for this symbiosis: the sea anemone Exaiptasia diaphana (‘Aiptasia’) and its native symbiont Breviolum minutum. In Chapter 2, I sought to determine the impact of decreased pH (7.68) on the ongoing health and maintenance of the cnidarian-dinoflagellate symbiosis. I coupled proteomics with a range of physiological measures to examine the responses of both Aiptasia and B. minutum. I found that, while decreased pH had little effect on physiological parameters, changes in the proteome expression of both partners indicated a cellular-level response to OA. In the dinoflagellate symbiont, the proteomic response to low pH was characterised by the relative over-abundance of photosynthesis-related proteins. These included six chlorophyll a-chlorophyll c2-peridinin-proteins, and Photosystem I and II reaction centre proteins active in chlorophyll binding and electron transfer in the light harvesting complexes, as well as the upregulation of heat shock proteins (HSPs), catalase and superoxide dismutase, with roles in reactive oxygen species (ROS) management. This photosynthetic activity was associated with an upregulation of central metabolic and biosynthetic processes, and the translocase H+-exporting diphosphatase, suggesting an increase in photosynthate transfer to the host anemone. Increased abundance of carbonic anhydrase 2 was observed in the host, implying an intensification of carbon concentrating mechanisms, which would support increased photosynthetic activity. In the anemone host, the proteomic data indicated an overall increase in cellular respiration and ATP synthesis at low pH, together with enhanced fatty acid synthesis, indicating a stimulatory effect of photosynthetically-derived nutrition. Over time, however, this benefit may also incur costs, as indicated by an apparent triggering of the host’s innate immune response – potentially driven by photosynthetically-derived ROS. Immune-response activation was signalled by increased abundance of alkaline phosphatases, an interferon-induced protein, collagen alpha chain, and a Golgi-associated plant pathogenesis-related protein, while HSPs, catalase and enolase indicated the upregulation of ROS management pathways. Interestingly, melanotransferrin, which is involved in cellular iron homeostasis, was downregulated in symbiotic host tissues over time. Iron is a key nutrient required for photosynthesis, and may imply that the anemones were restricting iron supply to their symbionts as a means of controlling population densities. Collectively, these findings suggest that, through the coordination of cellular processes, this model cnidarian-dinoflagellate symbiosis can likely acclimate to moderate OA exposure. In Chapter 3, I examined whether decreased pH (7.68 and 7.85) impacts the capacity of Aiptasia to acquire and establish a symbiosis with B. minutum. I found that low pH did not reduce symbiont uptake, colonisation rate, photosynthetic performance or final symbiont density during symbiosis establishment over four weeks, except where the symbiont was pre-exposed to reduced pH. In this case, there was an initial and short-term decrease in colonisation rate, followed by recovery. The implications for the health and availability of free-living Symbiodiniaceae populations, and any such delayed uptake in the early stages of colonisation are unknown and warrant further research. However, these data indicate that Aiptasia remains able to establish a functional symbiosis with B. minutum at low pH. This thesis indicates that soft-bodied cnidarians will be relatively resilient to future OA scenarios, and provides valuable insights to inform further work in reef-building corals. The findings presented here provide baselines from which to explore two under-researched aspects of OA impacts on the cnidarian-dinoflagellate symbiosis: responses at the cellular-level, and symbiont uptake and colonisation. To address the growing threat of climate change, further work is needed to understand cellular responses to OA, particularly during key life-stage events such as the establishment of symbiosis.

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Impact of Ocean Warming and Acidification on Symbiosis Establishment and Gene Expression Profiles in Recruits of Reef Coral Acropora intermedia

Cited by 15 publications

References 58 publications

Gregarious larval settlement mediates the responses of new recruits of the reef coral Acropora austera to ocean warming and acidification

Gregarious larval settlement mediates the responses of new recruits of the reef coral Acropora austera to ocean warming and acidification

The promotion of stress tolerant Symbiodiniaceae dominance in juveniles of two coral species due to simulated future conditions of ocean warming and acidification

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

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