Stomach microbiome simplification of a coral reef fish at its novel cold-range edge under climate change

Climate-driven range-extensions of animals into higher latitudes are often facilitated by phenotypic plasticity. Modifications to habitat preference, behaviour, and diet can increase the persistence of range-extending species in their novel high-latitude ecosystems. These strategies may be influenced by changes in in their gut and stomach microbial communities that are critical to host fitness, and potentially adaptive plasticity. Yet, it remains unknown if the gut and stomach microbiome of range-extending species is plastic in novel ranges to help facilitate these modifications. Here, we categorised stomach microbiome communities of a prevalent range-extending coral reef fish species along a 2,000-km latitudinal gradient in a global warming hotspot, extending from their tropical core-range to their novel temperate cold-range edge. At their cold-range edge, the coral reef fish’s stomach microbiome showed a 59% decrease in bacterial diversity, and a 164% increase in relative abundance of opportunistic bacteria (Vibrio) compared to their tropical core range. Microbiome diversity was unaffected by fish body size, water temperature, physiology (cellular defence and damage), and habitat type (turf, barren, oyster, kelp, and coral) across their range. The observed shifts in stomach microbiome composition suggests dysbiosis and low plasticity of tropical range-extending fishes to novel environmental conditions (e.g., temperate prey and lower seawater temperature) at their novel range edges, which may increase their susceptibility to disease in temperate ecosystems. We conclude that fishes extending their ranges to higher latitudes under ocean warming can experience a simplification (i.e. reduced diversity) of their stomach microbiome, which could restrict their current rate of range extensions or establishment in temperate ecosystems.

动物在向高纬度地区扩散的过程中，其范围扩展往往得益于表型可塑性。对栖息地偏好、行为和饮食的调整能够增强物种在其新型高纬度生态系统中的持久性。这些策略可能受到其肠道和胃部微生物群落的改变的影响，这些微生物群落对于宿主健康至关重要，并可能具有适应性可塑性。然而，目前尚不清楚，向新区域扩散的物种的肠道和胃部微生物群在新区域中是否具有可塑性，以促进这些改变。在本研究中，我们对一种普遍存在的范围扩展珊瑚礁鱼类的胃部微生物群落进行了分类，研究范围跨越了2,000公里的纬度梯度，从其热带核心区域延伸至其新型温带寒冷边缘。在寒冷边缘，珊瑚礁鱼的胃部微生物群落中细菌多样性下降了59%，而与热带核心区域相比，机会性细菌（如弧菌）的相对丰度增加了164%。在整个研究范围内，微生物群落多样性未受鱼类体型、水温、生理学（细胞防御和损伤）以及栖息地类型（草地、裸地、牡蛎、海藻和珊瑚）的影响。观察到的胃部微生物群落组成的转变表明，热带范围扩展鱼类在新型环境条件（如温带猎物和较低的海水温度）下可能存在菌群失调和低可塑性，这可能会增加其在温带生态系统中的疾病易感性。我们得出结论，在海洋变暖的背景下，鱼类向更高纬度扩展其范围可能会经历其胃部微生物群落的简化（即多样性降低），这可能会限制其当前的扩散速率或温带生态系统的定居。