Collaborative Research: Symbiosis as a fulcrum in a rapidly warming world

气候变化给地球上的居民带来了前所未有的挑战。了解气温上升如何影响生物的多样性和分布是至关重要的。然而，预测生物体对气候变化的反应是困难的，因为物种相互作用受到的影响不同于单个物种。这更加复杂，因为物种之间的相互作用往往涉及被称为共生体的“隐藏”微生物，这种微生物似乎特别容易受到气候变化的影响。海洋珊瑚的光合共生体就是例证，它们在海洋变暖期间被排出。气候对陆生系统中共生体介导的物种相互作用的影响知之甚少。研究这一现象的独特机会是使用具有良好特征的保护性共生的易处理蚜虫模型。蚜虫是植食性昆虫和重要的农业害虫，它们携带细菌共生体，保护它们免受病原体和寄生虫的侵害。先前的研究表明，一种广泛存在的抗寄生虫共生菌的大多数菌株在较暖的温度下无法保护蚜虫。但是来自这种共生体的其他菌株，以及来自第二种非必需共生体的菌株，在没有寄生虫的情况下，为蚜虫提供了对高温的耐受性——这似乎是通过拯救蚜虫生存所需的第三种共生体来实现的。将生物学实验与分子生物学、显微镜学、基因组学和基因表达研究相结合，pi将研究温度介导的共生失败机制，以及共生介导的气候适应能力的潜力。昆虫是最多样化的动物群体，而且大多数是共生的，所以蚜虫的发现很容易推广到大多数陆生动物。该奖项支持高中、本科和研究生研究人员的培训和专业发展，并包括社区外展活动。预测生物体对气候变化的反应是困难的，因为物种间的相互作用受到的影响不同于单个物种。更复杂的是，多细胞真核生物之间的相互作用往往是由微生物伴侣介导的，而微生物伴侣似乎特别容易受到热应激的影响。气候对微生物介导的物种相互作用的影响将通过一个高度可处理的蚜虫模型系统进行研究，该系统具有在基因型和表型水平上具有良好特征的防御性共生。先前的研究表明，一种广泛存在的抗寄生虫共生体——汉密尔顿菌的大多数菌株在较暖的温度下不能保护蚜虫。利用来自自然种群的常见菌株，笼式实验将验证以下假设：1)波动的温度维持了哈密通体的热相关遗传变异；2)在没有拟寄生虫的情况下，整体暴露在高温环境中，会选择具有热耐受性的菌株；3)在温暖温度和拟寄生虫的双重挑战下，会选择提供热坚固保护的菌株。其他检测将确定哈密尔顿菌功能的上限，以及另一种共生体沙雷氏菌是否在最热地区取代哈密尔顿菌。为了了解共生失败和恢复的机制，将对相关基因组进行测序，并检测共生对热胁迫的反应滴度、毒素的热不稳定性，以及是否通过拯救专性营养共生体Buchnera来产生热耐受性。这项研究增进了对气候对无处不在的昆虫可遗传共生体的影响的理解，对提供的许多有益服务以及对人类健康和农业构成的威胁产生了影响。该奖项反映了美国国家科学基金会的法定使命，并通过使用基金会的知识价值和更广泛的影响审查标准进行评估，被认为值得支持。

Climate change is creating unprecedented challenges for Earth’s inhabitants. It is critical to understand how rising temperatures affect the diversity and distributions of organisms. However, predicting organismal responses to climate change is difficult, because species interactions are impacted differently than individual species. This is further complicated because species interactions often involve ‘hidden’ microbes called symbionts, which appear especially vulnerable to climate change. This is exemplified by the photosynthesizing symbionts of marine corals, which are expelled during ocean warming. Less is known about climate impacts on symbiont-mediated species interactions in terrestrial systems. Unique opportunities to study this phenomenon occur using tractable aphid models with their well-characterized protective symbioses. Aphids are plant-feeding insects and important agricultural pests, which carry bacterial symbionts protecting them against pathogens and parasites. Prior work showed that most strains of a widespread anti-parasite symbiosis failed to protect aphids at warmer temperatures. But other strains from this symbiont, and from a second non-essential symbiont species, provided aphids with tolerance to high temperatures in the absence of parasites– plausibly by rescuing a third symbiont species required for aphid survival. Combining biological experiments with molecular biology, microscopy, genomics and gene expression studies, the PIs will study mechanisms of temperature-mediated symbiont failure and, conversely, the potential for symbiont-mediated climate resilience. Insects are the most diverse animal group, and most are symbiotic, so findings from aphids readily generalize to most terrestrial animals. This award supports the training and professional development of high school, undergraduate, graduate researchers, and includes community outreach events. Predicting organismal responses to climate change is difficult because species interactions are impacted differently than individual species. A further complication is that interactions among multicellular eukaryotes are often mediated by microbial partners, which appear especially vulnerable to thermal stress. Climate impacts on microbe-mediated species interactions will be investigated using a highly-tractable aphid model system with defensive symbioses that have been well-characterized at genotypic and phenotypic levels. Prior work showed that most strains of a widespread anti-parasitoid symbiont, Hamiltonella, fail to protect aphids at warmer temperatures. Using common strains derived from natural populations, cage experiments will test hypotheses that 1) fluctuating temperatures maintain thermally-relevant genetic variation in Hamiltonella, while 2) monolithic exposure to hot temperatures without parasitoids selects for thermal tolerance conferring strains, and 3) challenge with both warm temperatures and parasitoids selects for strains providing thermally-robust protection. Additional assays will define the upper limits of Hamiltonella function, and whether another symbiont, Serratia, replaces Hamiltonella in the hottest locales. To understand mechanisms of symbiont failure and resilience, relevant genomes will be sequenced coupled with assays examining symbiont titers in response to thermal stress, heat lability of toxins, and whether thermal tolerance occurs via rescue of the obligate nutritional symbiont Buchnera. This research enhances understanding of climate impacts on the ubiquitous heritable symbioses of insects, with implications for the many beneficial services provided, and threats to human health and agriculture posed.This award reflects NSF's statutory mission and has been deemed worthy of support through evaluation using the Foundation's intellectual merit and broader impacts review criteria.