Iron-oxidizer hotspots formed by intermittent oxic–anoxic fluid mixing in fractured rocks

Abstract

Subsurface environments host most of the fresh water on Earth as well as diverse microorganisms that may constitute a significant part of the biosphere. However, the dynamics and spatial distribution of subsurface microorganisms and their response to hydrological processes are poorly understood. Here we used chemical and metagenomic analyses of groundwater in a fractured rock aquifer in western France to determine the role of fractures in the formation of deep microbial hotspots in the subsurface. The majority of fractures, sampled in a 130-m-deep borehole, were anoxic, but a fracture carrying oxic groundwater was detected at 54-m depth, associated with a fivefold increase in the abundance of iron-oxidizing bacteria. We developed a mechanistic model of fluid flow and mixing in fractures and found that such microbial hotspots are sustained by the mixing of fluids with contrasting redox chemistries at intersections of fractures. The model predicts that metre-scale changes in near-surface water table levels cause intermittent oxygen delivery through deep fractures, which can extend the depth of the habitable zone for iron-oxidizing bacteria hundreds of metres into the subsurface. Given that fractures are ubiquitous at multiple scales in the subsurface, such deep microbial hotspots may substantially influence microbial communities and their effect on Earth’s biogeochemical cycles. Subsurface iron-oxidizing bacteria are sustained by intermittent oxygen delivery through rock fracture networks, according to biological and geochemical analyses of borehole fluids combined with a fluid mixing model.