Specific foraminiferal marker of the V9 18S rRNA gene. The estuarine quality paradox – eDNA metabarcoding provides a new vision of estuarine mudflats diversity

Environmental biomonitoring is a prerequisite for adapted and efficient evaluation of ecosystem degradation due to anthropogenic pressure or climate change. Among the different habitat, estuaries are efficient model as this ecotone is a crossroad of multiple anthropogenic and natural stressors. However, due to the multiple origins of stressors, the detection of anthropogenic pressure is challenging. The fact that in estuaries, abundant natural stressors often lead to negative quality assessments has been coined the “Estuarine quality paradox”. To solve this issue, the application of molecular approaches to successful bioindicators like Foraminifera is promising. However, the development and the validation of different sampling protocols, molecular procedures and data analyses remains to be completed before such a tool can be routinely applied. We conducted an environmental DNA survey of six estuaries along the French Atlantic coast, using a metabarcoding approach targeting foraminiferal clades. RDA analysis based on the distribution of 99 taxa showed that 40% of the variance was explained by the physical and chemical composition of the sediment and the climatic conditions. Our results demonstrate that estuarine environments possess a large stock of dormant or propagules stage with only a few taxa dominating the community composition. These findings underline the importance of the so called “rare biosphere” in estuarine ecosystems. Indeed, this diversity component in multiple stressor environments may constitute an important reservoir of species actively contributing to the community dynamics. Environmental DNA biomonitoring opens new perspectives to resolve the “estuarine quality paradox” by providing complementary information to the classical morphological approaches.

环境生物监测是针对人为压力或气候变化引发的生态系统退化，开展适应性且高效评估的先决条件。在各类生境中，河口（estuary）是极具研究价值的模型系统，因为这一生态交错带是多种人为与自然胁迫因子的交汇点。然而，由于胁迫因子来源多样，人为压力的精准识别颇具挑战。河口地区大量存在的自然胁迫因子往往会导致负面的生态质量评估，这一现象被称为“河口质量悖论（Estuarine quality paradox）”。为解决这一难题，将分子方法应用于有孔虫（Foraminifera）这类成熟生物指示物的研究路径颇具前景。然而，在这类工具得以常规应用之前，相关采样方案、分子实验流程与数据分析方法的开发与验证工作仍有待完善。本研究针对法国大西洋沿岸的6处河口开展了环境DNA（environmental DNA, eDNA）调查，采用靶向有孔虫类群的元条形码（metabarcoding）技术。基于99个分类单元分布的冗余分析（Redundancy Analysis, RDA）结果显示，40%的物种变异可由沉积物的理化性质与气候条件解释。本研究结果表明，河口环境中存在大量处于休眠或繁殖体阶段的生物，仅少数分类单元占据群落组成的主导地位。上述发现凸显了“稀有生物圈（rare biosphere）”在河口生态系统中的重要性。事实上，在多重胁迫环境中，这一多样性组分可能是积极参与群落动态的物种的重要储备库。环境DNA生物监测可为破解“河口质量悖论”提供全新研究视角，其通过为经典形态学方法提供补充信息。