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

Abstract

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.

Symbiont community changes confer fitness benefits for larvae, but not juveniles, in a vertically transmitting coral

“…Interestingly, we found Symbiodiniaceae community composition in M. digitata juveniles to be highly stable regardless of thermal exposure. This is in contrast to other studies in which shuffling in juvenile corals has been repeatedly confirmed during initial symbiont acquisition (Little et al 2004;Yorifuji et al 2017;Cumbo et al 2013;Cumbo et al 2013;Little et al 2004;Yorifuji et al 2017), and through development (Quigley et al 2017;2020;Terrell et al 2023), only stabilizing later in life (Abrego et al 2008). These changes through juvenile ontogeny are generally referred to as winnowing (Abrego et al 2008).…”

“…Assuming the community shift led to gains in heat tolerance, this suggests that either the maternal colonies or the larvae may be actively re-arranging their symbiont communities as an acclimatization mechanism to cope with heat stress. This mechanism has been seen in adults (Berkelmans and van Oppen 2006), eggs of vertical transmitters (Quigley et al 2019), and the juveniles of some coral species (Terrell et al 2023). The increased relative abundance of symbionts from the genera Symbiodinium, Durusdinium and Fugacium further supports this conjecture, as these are among the most stress tolerant genera (Swain et al 2017).…”

“…Life stage specific differences in physiology and symbiont community diversity in response to thermal stress Both larvae and juveniles were dominated by the same C15 DIV, but larvae survived much longer on average and their symbiont community composition showed greater differences under heat treatment than juveniles. There is ample evidence to show that symbiont communities drive host physiology in coral adults (Quigley et al 2022(Quigley et al , 2023Terrell et al 2023), underpinned by differences in symbiont tolerance to stress (Swain et al 2021). Symbiodinium microadriaticum and Durusdinium trenchii, for example, tend to produce less reactive oxygen species (ROS), a molecular response associated with coral bleaching, when exposed to heat stress compared to Breviolum minitum and Cladocopium goreaui, (Lesser 2019).…”

“…Increased abundance of symbionts in the opportunistic and generally stress tolerant genus Durusdinium is the canonical example of shuffling following heat stress (Berkelmans and van Oppen 2006;Quigley et al 2022), again emphasizing the role of symbionts in reef resilience (Berkelmans and van Oppen 2006;Quigley et al 2022). However, our knowledge of the functional relevance of shuffling and switching is generally limited to adult coral and has only been briefly examined in early life-history stages (Quigley et al 2019;Terrell et al 2023).…”

Screening for climate adaptative loci using seascape genomics resolves phenotypic variation in heat tolerance of the coral Acropora millepora.

“…In addition, the subclade C3 consists of several lineages that cannot be well resolved by ITS2 sequencing, among which a S. thermophilum variant was found in exceptionally warm environments in the Persian Arabian gulf 99 . Conversely, subclade C50 has been rarely observed in association with A. millepora although background levels have been reported in a recent study 100 . Interestingly, they found significant decrease in C50 abundance under increased temperatures suggesting that this subclade could be thermally sensitive.…”