The role of soil redox conditions in microbial phosphorus cycling in humid tropical forests

Humid tropical forests are among the most productive ecosystems globally, yet they often occur on soils with high phosphorus (P) sorption capacity, lowering P availability to biota. Short-term anoxic events are thought to release sorbed P and enhance its acquisition by soil microbes. However, the actual effects of anoxic conditions on microbial P acquisition in humid tropical forest soils are surprisingly poorly studied. We used laboratory incubations of bulk soils, NanoSIMS analysis of single microbial cells, and landscape scale measurements in the Luquillo Experimental Forest (LEF), Puerto Rico to test the hypothesis that anoxic conditions increase microbial P acquisition in humid tropical forests. In laboratory and field experiments we found that microbial P uptake generally decreased under anoxic conditions, leading to high microbial carbon (C) to P ratios in anoxic soils. The decreased P acquisition under anoxic conditions was correlated with lower microbial C use efficiency (CUE), an index of microbial energy transfer in ecosystems. Phosphorus amendments to anoxic soils led to increased microbial P uptake and higher CUE suggesting that microbes were less able to access and utilize P under natural low redox conditions. Under oxic conditions, microbial C:P ratios and CUE did not respond to changes in substrate stoichiometry. These results challenge the existing paradigm by showing that anoxic conditions can decrease microbial P uptake and ultimately constrain microbial CUE. Our findings indicate that soil redox conditions tightly couple soil P and C cycles and advance our understanding of controls on P cycling in humid tropical forest ecosystems. Support for this work was provided by grants BSR-8811902, DEB-9411973, DEB-9705814 , DEB-0080538, DEB-0218039 , DEB-0620910 , DEB-1239764, DEB-1546686, and DEB-1831952 from the National Science Foundation to the University of Puerto Rico as part of the Luquillo Long-Term Ecological Research Program. Additional support provided by the University of Puerto Rico and the International Institute of Tropical Forestry, USDA Forest Service.

湿润热带森林是全球生产力最高的生态系统之一，却常发育于磷（P）吸附容量极高的土壤中，导致生物可利用磷的含量大幅降低。此前学界普遍认为，短期缺氧事件可解吸土壤吸附态磷，增强土壤微生物对磷的获取能力。然而，学界对缺氧条件如何影响湿润热带森林土壤微生物磷获取过程的实际研究却极为匮乏。本研究以波多黎各卢奎略实验林（LEF）为研究样地，通过原状土壤室内培养、单微生物细胞纳米二次离子质谱（NanoSIMS）分析以及景观尺度原位观测，验证了“缺氧环境可提升湿润热带森林微生物磷获取能力”这一假说。室内培养与野外实验结果均显示，缺氧条件下微生物的磷吸收量普遍下降，使得缺氧土壤的微生物碳（C）磷比显著升高。缺氧环境下微生物磷获取能力的下降，与更低的微生物碳利用效率（CUE，生态系统微生物能量传递的关键指标）显著相关。向缺氧土壤施加磷素后，微生物的磷吸收量与碳利用效率均显著提升，表明在自然低氧化还原条件下，微生物对磷的获取与利用能力受到限制。而在有氧环境中，微生物碳磷比与碳利用效率并未随底物化学计量比的变化产生响应。本研究结果挑战了现有主流认知范式：缺氧环境反而会降低微生物的磷吸收能力，并最终限制其碳利用效率。本研究结果表明，土壤氧化还原状态可紧密耦合土壤磷循环与碳循环，这一发现加深了我们对湿润热带森林生态系统磷循环调控机制的理解。本研究得到美国国家科学基金会（National Science Foundation）向波多黎各大学提供的多项研究基金资助，基金编号包括BSR-8811902、DEB-9411973、DEB-9705814、DEB-0080538、DEB-0218039、DEB-0620910、DEB-1239764、DEB-1546686及DEB-1831952，相关工作属于卢奎略长期生态研究计划的一部分。此外，本研究还得到波多黎各大学与美国农业部林业局国际热带林业研究所的额外支持。