Supporting data for "Coral-Algal Symbiosis Through Stress and Recovery"

Coral-Algal Symbiosis Through Stress and Recovery It’s thought that almost every organism on the planet partakes in mutualistic associations, though few so prominently as reef-building coral. An evolutionarily successful relationship, endosymbiotic algae (family Symbiodiniaceae) support coral metabolism by provisioning photosynthetic nutrients, in return for shelter and access to nitrogenous waste products. Central to this success is the idea that the costs of contributing to a partners fitness must be outweighed by the benefits gained, which, under normal circumstances, is the case for the coral-algal relationship. Coral hosts may even actively protect their own investment by rationing the nitrogen access and expelling excess algal cells, maintaining a sustainable population of Symbiodiniaceae. Unfortunately, adverse environmental conditions disrupt this delicate balance – promoting symbiont nutrient hoarding or the breakdown of photosynthesis – and cause corals to bleach, in a phenomenon that threatens coral reef ecosystems worldwide.While a large body of literature has focused on what happens up to and during bleaching in an attempt to prevent these devastating effects, researchers have more recently shifted their focus to post-bleaching recovery. For example, a driving question is whether introducing experimentally evolved Symbiodiniaceae into bleached adult corals may improve their resistance and resilience to further stress. To that end, it’s imperative to understand a) are recovering corals capable of forming novel, sustainable associations and b) do they function like a healthy mutualism?In this thesis, I explore the influence of natural and introduced Symbiodiniaceae diversity on the stress tolerance and subsequent recovery of reef-building coral. Firstly, I leverage natural symbiont diversity of Acropora millepora from distinct habitats across the Great Barrier Reef to investigate how environment and symbiont identify interact to shape tolerance. I demonstrate that more tolerant Symbiodiniaceae can form successful and comparable mutualism to generalist species, and that symbiont identity alone may not predict coral resistance. I further show how stable isotope tracers, including novel incorporation of 2H, can be used detect sub-lethal indicators of heat stress, particularly early damage to photosynthetic apparatus. I then shift the lens to coral recovery, presenting gene expression profiles of bleached Galaxea fascicularis following exposure to Cladocopium goreaui, Durusdinium trenchii or a mixture of both. Despite initial uptake, regional specificity may limit their capacity for establishing novel Symbiodiniaceae communities. This reiterates challenges for large-scale application of symbiont manipulation as a way to bolster coral resilience. Finally, I combine bulk and compound-specific stable isotope analysis to compare nutrient exchange in a healthy G. fascicularis mutualism and those recovering under variable environmental conditions. I explore host vs symbiont-centric recovery strategies and determine that while the quantity of shared nutrients is consistent between recovering and healthy holobionts, the quality is not. Reduced translocation of essential amino acids may enhance the vulnerability of corals throughout recovery, highlighting the value of comprehensive methods when quantifying the function of coral-algal symbiosis. Building foundational knowledge of how corals and their Symbiodiniaceae in this way will not only aid in defining natural association, but also improve the design and success of potential interventions.

胁迫与恢复过程中的珊瑚-藻类共生关系

学界普遍认为，地球上几乎所有生物都存在互利共生关系，但造礁珊瑚的共生关系尤为突出。作为演化上的成功策略，内共生藻类（Symbiodiniaceae科）通过为珊瑚提供光合营养物质支撑其新陈代谢，以此换取栖息场所与含氮代谢废物的获取权。这一共存关系演化成功的核心逻辑在于：为提升共生伙伴的适合度所付出的成本，必须低于从中获取的收益；在正常环境下，珊瑚与藻类的共生关系恰好符合这一准则。珊瑚宿主甚至会主动守护自身的共生投资：通过调控氮元素供给、排出过量藻类细胞，以此维持Symbiodiniaceae种群的可持续规模。

然而，恶劣的环境条件会打破这一精妙的平衡：促进共生藻囤积营养物质或破坏光合作用，进而引发珊瑚白化，这一现象正威胁着全球范围内的珊瑚礁生态系统。尽管已有大量研究聚焦于白化发生前及白化过程中的机制，以期规避这些毁灭性影响，但近年来研究者们已将目光转向白化后的恢复阶段。例如，当前的核心研究问题之一是：将经实验演化的Symbiodiniaceae接种至已白化的成年珊瑚体内，能否提升其对后续胁迫的抗性与恢复力？

为此，我们亟需厘清两个核心问题：其一，正在恢复的珊瑚能否建立全新且可持续的共生关系？其二，恢复中的珊瑚是否能如健康共生体般发挥功能？

本论文探究了天然与外源Symbiodiniaceae的多样性对造礁珊瑚胁迫耐受性及其后续恢复过程的影响。首先，本研究利用大堡礁不同生境中采集的多孔鹿角珊瑚（Acropora millepora）的天然共生藻多样性，探究环境因子与共生藻身份如何共同调控珊瑚的胁迫耐受性。研究结果表明，耐受性更强的Symbiodiniaceae可建立与广适性物种相当的成功共生关系，且仅依靠共生藻身份无法准确预测珊瑚的胁迫抗性。本研究还证实，包括新型氘（²H）标记在内的稳定同位素示踪技术，可用于检测热胁迫的亚致死性指标，尤其是光合系统的早期损伤。

随后，本研究将视角转向珊瑚恢复过程，报告了白化的杯形珊瑚（Galaxea fascicularis）分别接种Cladocopium goreaui、Durusdinium trenchii以及二者混合菌群后的基因表达谱。尽管珊瑚可初步吸收这些共生藻，但区域特异性可能会限制其建立全新Symbiodiniaceae群落的能力。这一结果进一步凸显了将共生藻调控技术大规模应用以提升珊瑚恢复力所面临的挑战。

最后，本研究结合整体稳定同位素分析与化合物特异性稳定同位素分析，对比了健康杯形珊瑚共生体与在多变环境条件下恢复的共生体之间的营养交换模式。本研究还探究了以宿主为中心与以共生藻为中心的恢复策略，并发现：恢复中与健康全共生体之间的共享营养物质总量保持一致，但营养质量存在差异。必需氨基酸的转运量降低，可能会加剧珊瑚在恢复过程中的脆弱性，这也凸显了采用综合方法量化珊瑚-藻类共生功能的重要价值。

通过此类研究积累珊瑚与其Symbiodiniaceae共生关系的基础认知，不仅有助于明确天然共生关系的内在机制，还能为优化潜在干预手段的设计与提升其成功率提供支撑。