pH and exchangeable aluminum are major regulators of microbial energy flow and carbon use efficiency in soil microbial communities

The microbial partitioning of organic carbon (C) into either anabolic (i.e. growth) or catabolic (i.e. respiration) metabolic pathways represents a key process regulating the amount of added C that is retained in soil. The factors regulating C use efficiency (CUE) in agricultural soils, however, remain poorly understood. The aim of this study was to investigate substrate CUE from a wide range of soils (n = 970) and geographical area (200,000 km2) to determine which soil properties most influenced C retention within the microbial community. Using a 14C-labeling approach, we showed that the average CUE across all soils was 0.65 ± 0.003, but that the variation in CUE was relatively high within the sample population (CV 14.9%). Of the major properties measured in our soils, we found that pH and exchangeable aluminum (Al) were highly correlated with CUE. We identified a critical pH transition point at which CUE declined (pH 5.5). This coincided exactly with the point at which Al3+ started to become soluble. In contrast, other soil factors e.g. total C and nitrogen (N), dissolved organic C (DOC), clay content, available calcium, phosphorus (P) and sulfur (S), total base cations showed little or no relationship with CUE. We also found no evidence to suggest that nutrient stoichiometry (C:N, C:P and C:S ratios) influenced CUE in these soils. Based on current evidence, we postulate that the decline in microbial CUE at low pH and high Al reflects a greater channeling of C into energy intensive metabolic pathways involved in overcoming H+/Al3+ stress (e.g. cell repair and detoxification). The response may also be associated with shifts in microbial community structure, which are known to be tightly associated with soil pH. We conclude that maintaining agricultural soils above pH 5.5 maximizes microbial energy efficiency.