Fadum J M, Borton M A, Daly R A, Wrighton K C, Hall E K
Graduate Degree Program in Ecology, Colorado State University, Fort Collins, Colorado, USA.
Department of Ecosystem Science and Sustainability, Colorado State University, Fort Collins, Colorado, USA.
mSystems. 2024 Feb 20;9(2):e0105923. doi: 10.1128/msystems.01059-23. Epub 2024 Jan 23.
Nitrogen (N) availability is one of the principal drivers of primary productivity across aquatic ecosystems. However, the microbial communities and emergent metabolisms that govern N cycling in tropical lakes are both distinct from and poorly understood relative to those found in temperate lakes. This latitudinal difference is largely due to the warm (>20°C) temperatures of tropical lake anoxic hypolimnions (deepest portion of a stratified water column), which result in unique anaerobic metabolisms operating without the temperature constraints found in lakes at temperate latitudes. As such, tropical hypolimnions provide a platform for exploring microbial membership and functional diversity. To better understand N metabolism in warm anoxic waters, we combined measurements of geochemistry and water column thermophysical structure with genome-resolved metatranscriptomic analyses of the water column microbiome in Lake Yojoa, Honduras. We sampled above and below the oxycline in June 2021, when the water column was stratified, and again at the same depths and locations in January 2022, when the water column was mixed. We identified 335 different lineages and significantly different microbiome membership between seasons and, when stratified, between depths. Notably, (indicative of dissimilatory nitrate reduction to ammonium) was upregulated relative to other N metabolism genes in the June hypolimnion. This work highlights the taxonomic and functional diversity of microbial communities in warm and anoxic inland waters, providing insight into the contemporary microbial ecology of tropical ecosystems as well as inland waters at higher latitudes as water columns continue to warm in the face of global change.IMPORTANCEIn aquatic ecosystems where primary productivity is limited by nitrogen (N), whether continuously, seasonally, or in concert with additional nutrient limitations, increased inorganic N availability can reshape ecosystem structure and function, potentially resulting in eutrophication and even harmful algal blooms. Whereas microbial metabolic processes such as mineralization and dissimilatory nitrate reduction to ammonium increase inorganic N availability, denitrification removes bioavailable N from the ecosystem. Therefore, understanding these key microbial mechanisms is critical to the sustainable management and environmental stewardship of inland freshwater resources. This study identifies and characterizes these crucial metabolisms in a warm, seasonally anoxic ecosystem. Results are contextualized by an ecological understanding of the study system derived from a multi-year continuous monitoring effort. This unique data set is the first of its kind in this largely understudied ecosystem (tropical lakes) and also provides insight into microbiome function and associated taxa in warm, anoxic freshwaters.
氮(N)的可利用性是影响水生生态系统初级生产力的主要驱动因素之一。然而,与温带湖泊相比,热带湖泊中控制氮循环的微生物群落和新兴代谢过程既不同又鲜为人知。这种纬度差异主要是由于热带湖泊缺氧温跃层(分层水柱的最深处)温度较高(>20°C),这导致独特的厌氧代谢过程不受温带湖泊温度限制的影响。因此,热带温跃层为探索微生物组成和功能多样性提供了一个平台。为了更好地理解温暖缺氧水域中的氮代谢,我们将地球化学和水柱热物理结构的测量与洪都拉斯约霍亚湖水柱微生物群落的基因组解析宏转录组分析相结合。我们在2021年6月水柱分层时,在氧化跃层上方和下方进行了采样,并于2022年1月在相同深度和位置再次采样,此时水柱处于混合状态。我们鉴定出335个不同的谱系,且季节之间以及分层时不同深度之间的微生物群落组成存在显著差异。值得注意的是,在6月的温跃层中,相对于其他氮代谢基因,(异化硝酸盐还原为铵的指示基因)表达上调。这项工作突出了温暖缺氧内陆水域中微生物群落的分类和功能多样性,为热带生态系统以及高纬度内陆水域在面对全球变化时水柱持续变暖情况下的当代微生物生态学提供了见解。重要性在初级生产力受氮(N)限制的水生生态系统中,无论是持续、季节性限制还是与其他养分限制共同作用,无机氮可利用性的增加都可能重塑生态系统结构和功能,可能导致富营养化甚至有害藻华。虽然矿化和异化硝酸盐还原为铵等微生物代谢过程会增加无机氮的可利用性,但反硝化作用会从生态系统中去除生物可利用的氮。因此,了解这些关键的微生物机制对于内陆淡水资源的可持续管理和环境 stewardship 至关重要。本研究在一个温暖、季节性缺氧的生态系统中识别并表征了这些关键代谢过程。研究结果通过对该研究系统多年连续监测所获得的生态学理解进行了背景化。这个独特的数据集在这个研究较少的生态系统(热带湖泊)中尚属首次,也为温暖缺氧淡水中的微生物群落功能及相关分类群提供了见解。