Microbial hydrogen cycling in agricultural systems - plant beneficial or detrimental?

Abstract

Hydrogen-oxidising bacteria play a key role in maintaining the composition of gases within the atmosphere and are ubiquitous in agricultural soils. While studies have shown that hydrogen accumulates in soil surrounding legume nodules and the soil surface, soils as a whole act as a net sink for hydrogen, raising questions about how hydrogen is internally recycled by soils. Can the energy derived from hydrogen oxidation be directly funnelled into plants to promote their growth or does it only act as a booster for other plant-growth promoting bacteria? Moreover, while the fertilisation effect of hydrogen on plants has previously been shown to be beneficial, questions remain about the upper limit of hydrogen uptake by plants before it becomes detrimental. Agricultural practices such as fertilisation may impact the balance of hydrogen-oxidisers and hydrogen-producers in these ecosystems, potentially having detrimental effects on not only agricultural land but also global biogeochemical cycles. In this perspectives piece, we highlight the importance of understanding the contribution of hydrogen to agricultural soils and the effects of agricultural practices on the ability for bacteria to cycle hydrogen in agricultural soils. We propose a framework to gain better insights into microbial hydrogen cycling within agroecosystems, which could contribute to the development of new agricultural biotechnologies.

FIGURE 1

Overview of microbial hydrogen cycling within agricultural soils and predicted pathways of hydrogen removal from soil. (A) The concentration of hydrogen is maintained at approximately 0.53 parts per million by volume (ppmv) through various hydrogen production and removal processes in the soil. Hydrogen input into the soil microbial hydrogen cycle includes via hydrogen deposition from the atmosphere (indicated by the light blue arrow), nitrogen (N₂) fixation and fermentation reactions (light green arrow). The produced hydrogen can then be taken up by hydrogen oxidising bacteria or by plants (dark green arrows) or it can be emitted into the atmosphere (dark blue arrow). (B) Proposed mechanisms of bacteria‐mediated soil hydrogen cycling. Hydrogen is produced as a by‐product of nitrogen fixation by nitrogenase enzymes (Nif). The excess hydrogen can then potentially be removed either through an internal hydrogen uptake hydrogenase (Hup) or by neighbouring bacteria that contain either a high affinity (e.g. Hhy) or low affinity (e.g. Hup) hydrogenase. (C) Proposed mechanisms by which hydrogen fertilisation occurs in crops. The direct effects of molecular hydrogen on crops include greater root elongation, increased plant biomass and improved resistance to drought and reactive oxygen species (ROS)‐mediated stress. Indirect effects include downstream effects of hydrogen oxidation on plant growth promoting rhizobacteria including greater phosphate solubilisation, siderophore and 1–aminocyclopropane–1–carboxylate (ACC) deaminase production. Figure created using BioRender.