Table_1_Changes in Carbon Oxidation State of Metagenomes Along Geochemical Redox Gradients.XLSX

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.

对地球化学如何影响微生物群落基因组组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涉猎。本研究系统地记录了碳氧化态的变化，该指标源自生物大分子序列的化学公式，并利用了18项研究发表的宏基因组学和宏转录组学数据集，这些研究代表了不同的海洋和陆地环境。我们发现，DNA的碳氧化态以及从编码序列推断出的蛋白质的碳氧化态，都遵循与黄石国家公园（美国）热泉流体混合和冷却相关的地球化学红氧梯度。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的碳氧化态与海洋缺氧区的氧气浓度呈负相关。在这种情况下，热力学模型不可行，但靠近海洋表面的DNA低碳氧化态反映了低GC含量，这可以归因于适应低营养条件生物的基因组简化。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（AT富集）的细胞外DNA的选择性降解而发生的DNA改变有关。沉积物表现出更为复杂的特性，碳氧化态在硫酸盐-甲烷转换区附近达到最小值，并在深度增加时再次上升；显著更高的氧化态还与富含铁氧化物且有机碳含量低的波罗的海古老淡水主导沉积物相关。这一关于碳氧化态的地球生物化学研究揭示了宏基因组序列中环境信息的全新方面，并为未来可能使用古代DNA序列作为古红氧指标的研究提供了参考框架。