Pfab Ferdinand, Detmer A Raine, Moeller Holly V, Nisbet Roger M, Putnam Hollie M, Cunning Ross
Department of Ecology, Evolution and Marine Biology, University of California, Santa Barbara, CA USA.
Department of Biological Sciences, University of Rhode Island, Kingston, RI USA.
Coral Reefs. 2024;43(6):1627-1645. doi: 10.1007/s00338-024-02561-1. Epub 2024 Oct 30.
The coral-dinoflagellate endosymbiosis is based on nutrient exchanges that impact holobiont energetics. Of particular concern is the breakdown or dysbiosis of this partnership that is seen in response to elevated temperatures, where loss of symbionts through coral bleaching can lead to starvation and mortality. Here we extend a dynamic bioenergetic model of coral symbioses to explore the mechanisms by which temperature impacts various processes in the symbiosis and to enable simulational analysis of thermal bleaching. Our model tests the effects of two distinct mechanisms for how increased temperature impacts the symbiosis: 1) accelerated metabolic rates due to thermodynamics and 2) damage to the photosynthetic machinery of the symbiont caused by heat stress. Model simulations show that the model can capture key biological responses to different levels of increased temperatures. Moderately increased temperatures increase metabolic rates and slightly decrease photosynthesis. The slightly decreased photosynthesis rates cause the host to receive less carbon and share more nitrogen with the symbiont. This results in temporarily increased symbiont growth and a higher symbiont/host ratio. In contrast, higher temperatures cause a breakdown of the symbiosis due to escalating feedback that involves further reduction in photosynthesis and insufficient energy supply for concentration by the host. This leads to the accumulation of excess light energy and the generation of reactive oxygen species, eventually triggering symbiont expulsion and coral bleaching. Importantly, bleaching does not result from accelerated metabolic rates alone; it only occurs as a result of the photodamage mechanism due to its effect on nutrient cycling. Both higher light intensities and higher levels of DIN render corals more susceptible to heat stress. Conversely, heterotrophic feeding can increase the maximal temperature that can be tolerated by the coral. Collectively these results show that a bioenergetics model can capture many observed patterns of heat stress in corals, such as higher metabolic rates and higher symbiont/host ratios at moderately increased temperatures and symbiont expulsion at strongly increased temperatures.
The online version contains supplementary material available at 10.1007/s00338-024-02561-1.
珊瑚与甲藻的内共生关系基于影响共生体能量学的营养物质交换。特别值得关注的是这种共生关系的破坏或失调，在温度升高时会出现这种情况，珊瑚白化导致共生体丧失会引发饥饿和死亡。在此，我们扩展了珊瑚共生的动态生物能量模型，以探究温度影响共生中各种过程的机制，并实现对热白化的模拟分析。我们的模型测试了温度升高影响共生的两种不同机制的效果：1）由于热力学导致的代谢率加速；2）热应激对共生体光合机构的损害。模型模拟表明，该模型能够捕捉到对不同程度温度升高的关键生物学反应。适度升高的温度会提高代谢率并略微降低光合作用。光合作用速率的略微降低导致宿主接收的碳减少，并与共生体共享更多的氮。这导致共生体生长暂时增加以及共生体/宿主比例升高。相比之下，更高的温度会导致共生关系的破坏，这是由于不断升级的反馈，包括光合作用的进一步降低以及宿主用于浓缩的能量供应不足。这会导致过量光能的积累和活性氧物种的产生，最终引发共生体排出和珊瑚白化。重要的是，白化并非仅由代谢率加速导致；它仅因光损伤机制对营养循环的影响而发生。更高的光照强度和更高水平的溶解无机氮都会使珊瑚更容易受到热应激的影响。相反，异养摄食可以提高珊瑚能够耐受的最高温度。总体而言，这些结果表明生物能量模型能够捕捉到许多在珊瑚中观察到的热应激模式，例如在适度升高的温度下更高的代谢率和更高的共生体/宿主比例，以及在温度大幅升高时共生体排出。
在线版本包含可在10.1007/s00338-024-02561-1获取的补充材料。
