Mechanism and capacity of black carbon (biochar) to support microbial growth

Abstract

Black carbon has been shown to suppress microbial methane production by promoting anaerobic oxidation of organic carbon, diverting electrons from methanogenesis. This finding represents a new process through which black carbon, such as wildfire char and biochar, can impact the climate. However, the mechanism and capacity of black carbon to support metabolism remained unclear. We hypothesized black carbon could support microbial growth exclusively through its electron storage capacity (ESC). The electron contents of a wood biochar was quantified through redox titration with titanium(III) citrate before and after Geobacter metallireducens growth, with acetate as an electron donor and air-oxidized biochar as an electron acceptor. Cell number increased 42-fold, from 2.8(± 0.6) × 10⁸ to 1.17(± 0.14) × 10¹⁰, in 8 days based on fluorescent cell counting and the result was confirmed by qPCR. The qPCR results also showed that most cells existed in suspension, whereas cell attachment to biochar was minimal. Graphite, which conducts but does not store electrons, did not support growth. Through electron balance and use of singly ¹³C-labeled acetate (¹³CH₃COO^–), we showed (1) G. metallireducens could use 0.86 mmol/g, or ~ 19%, of the biochar's ESC for growth, (2) 84% and 16% of the acetate was consumed for energy and biosynthesis, respectively, during biochar respiration and (3) ca. 80 billion electrons were deposited into biochar for each cell produced. This is the first study to establish electron balance for microbial respiration of black carbon and to quantitatively determine the mechanism and capacity of biochar-supported growth.

Graphical Abstract