Data_Sheet_2_Changes in Carbon Oxidation State of Metagenomes Along Geochemical Redox Gradients.pdf

There is widespread interest in how geochemistry affects the genomic makeup of microbial communities, but the possible impacts of oxidation-reduction (redox) conditions on the chemical composition of biomacromolecules remain largely unexplored. Here we document systematic changes in the carbon oxidation state, a metric derived from the chemical formulas of biomacromolecular sequences, using published metagenomic and metatranscriptomic datasets from 18 studies representing different marine and terrestrial environments. We find that the carbon oxidation states of DNA, as well as proteins inferred from coding sequences, follow geochemical redox gradients associated with mixing and cooling of hot spring fluids in Yellowstone National Park (USA) and submarine hydrothermal fluids. Thermodynamic calculations provide independent predictions for the environmental shaping of the gene and protein composition of microbial communities in these systems. On the other hand, the carbon oxidation state of DNA is negatively correlated with oxygen concentration in marine oxygen minimum zones. In this case, a thermodynamic model is not viable, but the low carbon oxidation state of DNA near the ocean surface reflects a low GC content, which can be attributed to genome reduction in organisms adapted to low-nutrient conditions. We also present evidence for a depth-dependent increase of oxidation state at the species level, which might be associated with alteration of DNA through horizontal gene transfer and/or selective degradation of relatively reduced (AT-rich) extracellular DNA by heterotrophic bacteria. Sediments exhibit even more complex behavior, where carbon oxidation state minimizes near the sulfate-methane transition zone and rises again at depth; markedly higher oxidation states are also associated with older freshwater-dominated sediments in the Baltic Sea that are enriched in iron oxides and have low organic carbon. This geobiochemical study of carbon oxidation state reveals a new aspect of environmental information in metagenomic sequences, and provides a reference frame for future studies that may use ancient DNA sequences as a paleoredox indicator.

当前对地化性质如何影响微生物群落基因组构成的研究引起了广泛关注，然而，氧化还原（红氧）条件对生物大分子化学组成可能产生的影响却鲜有深入探讨。本研究系统地记录了通过生物大分子序列化学公式推导出的碳氧化态这一指标的变化，利用18项不同海洋和陆地环境的已发表宏基因组学和宏转录组学数据集。研究发现，DNA以及从编码序列推断出的蛋白质的碳氧化态，均遵循与黄石国家公园（美国）热水流体混合和冷却以及海底热液流体相关的地化红氧梯度。热力学计算为这些系统中微生物群落基因和蛋白质组成的生态环境塑造提供了独立的预测。另一方面，DNA的碳氧化态与海洋氧最小浓度区中的氧气浓度呈负相关。在这种情况下，热力学模型并不可行，但靠近海洋表面的DNA低碳氧化态反映了GC含量较低，这可以归因于适应低营养条件生物体的基因组缩减。我们还提供了物种水平上氧化态随深度增加的证据，这可能与其通过水平基因转移和/或异养细菌对相对还原的（AT富集的）胞外DNA的选择性降解而导致的DNA改变有关。沉积物表现出更为复杂的行为，其碳氧化态在硫酸盐-甲烷转换区附近达到最小值，而在深处又上升；显著更高的氧化态也与富含氧化铁且有机碳含量低的波罗的海古老淡水主导沉积物有关。此碳氧化态的地生物化学研究揭示了宏基因组序列中环境信息的另一新维度，并为未来可能使用古代DNA序列作为古红氧指示剂的科研工作提供了参考框架。