Geological activity shapes the microbiome in deep-subsurface aquifers by advection

Abstract

Subsurface environments host diverse microorganisms in fluid-filled fractures; however, little is known about how geological and hydrological processes shape the subterranean biosphere. Here, we sampled three flowing boreholes weekly for 10 mo in a 1478-m-deep fractured rock aquifer to study the role of fracture activity (defined as seismically or aseismically induced fracture aperture change) and advection on fluid-associated microbial community composition. We found that despite a largely stable deep-subsurface fluid microbiome, drastic community-level shifts occurred after events signifying physical changes in the permeable fracture network. The community-level shifts include the emergence of microbial families from undetected to over 50% relative abundance, as well as the replacement of the community in one borehole by the earlier community from a different borehole. Null-model analysis indicates that the observed spatial and temporal community turnover was primarily driven by stochastic processes (as opposed to deterministic processes). We, therefore, conclude that the observed community-level shifts resulted from the physical transport of distinct microbial communities from other fracture(s) that outpaced environmental selection. Given that geological activity is a major cause of fracture activity and that geological activity is ubiquitous across space and time on Earth, our findings suggest that advection induced by geological activity is a general mechanism shaping the microbial biogeography and diversity in deep-subsurface habitats across the globe.

Comparison of Microbial Profiling and Tracer Testing for the Characterization of Injector-Producer Interwell Connectivities

“…Microbial processes in subsurface reservoirs can be classified into two major categories: metabolic [6,7,[12][13][14][15][16] and hydrodynamic [17][18][19] (subcategories of deterministic process and stochastic process in microbial ecology [20][21][22], respectively). Metabolic processes refer to the change in microbial community composition after disturbance to reservoir environmental conditions (e.g., ionic concentrations, oxygen level, organic carbon availability, etc.)…”

“…Metabolic processes refer to the change in microbial community composition after disturbance to reservoir environmental conditions (e.g., ionic concentrations, oxygen level, organic carbon availability, etc.) because different taxa have different physiologies, metabolic capabilities, and hence different levels of fitness to the changed environment [18,23]. For example, in aquifer systems, recharge events can significantly shift groundwater microbial communities by altering groundwater hydrochemical properties and stimulating the growth of opportunistic microbes [17,24,25].…”

“…Hydrodynamic processes, on the other hand, refer to the passive dispersal capacity of microbial cells along with fluid flow because of their small body sizes. In deep, fractured aquifers where the energy-limited environment permits only extremely slow cell metabolism [26,27], natural or human-induced shifts in groundwater mixing could lead to variations in fluid-associated microbial community structure primarily by advective transport [18]. In shallow geological formations, hydrodynamic process can play important roles in microbial community dynamics as well [17,19].…”

“…A reservoir can be water-based (e.g., groundwater and geothermal) or hydrocarbon-based (e.g., oil fields and shale). Reservoir operation can involve production of reservoir fluids under natural formation pressure or by pumping (i.e., primary production) [4], water injection to displace reservoir fluids out of a different well and/or hydraulically stimulate reservoir permeability (i.e., interwell displacement) [6,18], and injection/flowback into/from a single well (i.e., single well push-pull) [7]. A better understanding of the spatial and temporal patterns of microbial community structure under different scenarios provides not only grounds for utilizing microbial data for improved resource management, but also valuable insights for deep biosphere ecology research.…”

“…In this study, we analyzed the microbial community composition alongside four artificial tracer tests during a long-term flow test at a deep-subsurface aquifer with sparse permeable fractures. The repeated tracer tests were conducted in order to characterize the evolution of the interwell permeable fracture network over time [18,[28][29][30]. Performed on or near the same date of microbial community analyses, the tracer test results also provided useful information for microbial data interpretation from a hydrodynamic perspective.…”