Differential structure and functional gene response to geochemistry associated with the suspended and attached shallow aquifer microbiomes from the Illinois Basin, IL

Authors: DONG, YIRAN - China University Of Geosciences; SANFORD, ROBERT - University Of Illinois; Connor, Lynn; Chee Sanford, Joanne; WIMMER, BRACKEN - Illinois State Geological Survey; IRANMANESH, ABBAS - Illinois State Geological Survey; SHI, LIANG - China University Of Geosciences; KRAPAC, IVAN - Illinois State Geological Survey; LOCKE, RANDALL - Illinois State Geological Survey; SHAO, HONGBO - Illinois State Geological Survey

Submitted to: Water Research
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 7/8/2021
Publication Date: 7/14/2021
Citation: Dong, Y., Sanford, R.A., Connor, L.M., Chee-Sanford, J.C., Wimmer, B.T., Iranmanesh, A., Shi, L., Krapac, I.G., Locke, R.A., Shao, H. 2021. Differential structure and functional gene response to geochemistry associated with the suspended and attached shallow aquifer microbiomes from the Illinois Basin, IL. Water Research. 202. Article 117431. https://doi.org/10.1016/j.watres.2021.117431.
DOI: https://doi.org/10.1016/j.watres.2021.117431

Interpretive Summary: Microorganisms in nature live either in suspension or attached to surfaces. In soil environments, suspended microbes move with water and occupy pore spaces between soil particles. Microbial attachments in soil, however, vary with the type of surfaces available, including soil particles, root and plant tissues, seeds, other macrobiotic life, and plant detritus. What processes influence the formation of communities to be attached or remain suspended has recently been better addressed with the development of new molecular methods used to sequence members of the community. This project used a natural aquifer system to evaluate spatial and temporal changes in suspended and attached microbial communities, with results that may extend to theory that might relate to patterns of microbial communities that form on e.g. plant roots. The approach used here combined geochemical data analyzed with gene amplification and sequencing. The results showed distinct dominating populations changing over time and space, with the composition of communities emerging distinct between suspended vs. attached environments, but assemblies of population types in either compartment largely depended on the localized environmental conditions. The significance of this study demonstrates the response between microbial communities and their immediate environment is controlled by multiple factors, including both directed and random processes. This significance may be extended to more complex relationships involving microbial communities, soil, and plants all together, however, identifying unifying principles may be more difficult due to the complexity. This may be possible to achieve in such systems using a similar holistic approach as modeled in this study, which combines biochemical processes with the emerging genetic and functional activities of the microbial assemblies that ultimately form in these relationships.

Technical Abstract: Subsurface microbiomes are of fundamental and practical significance, while our understandings about the differentially distributed subsurface microbial communities associated with aquifer (suspended) and bedrock (attached), functionalities, and the influential processes controlling their assembly in this unique ecosystem have been limited. In this study, an efficient pipeline combining geochemistry, high-throughput FluidigmTM functional gene amplification and sequencing was developed to analyze the suspended and attached microbial communities inhabiting five shallow groundwater wells monitoring two geological formations of the Illinois Basin, IL, USA. With distinct dominating taxa enriched in either phase, the suspended and the attached microbial communities exhibited significantly different spatial and temporal changes in richness and composition. Further analyses of the representative functional genes (i.e., nifH, pmoA, dsrB, and aprA) affiliated with N2 fixation, methane oxidation, and sulfate reduction, respectively, suggested functional redundancy of the subsurface microbiomes. In addition, the spatial and temporal changes in the diversity, composition and distribution of the functional genes in response to the environmental conditions varied between specific genes and sample types (suspended vs. attached). Notably, the deterministic and stochastic ecological processes shaped the assembly of microbial communities and functional gene reservoirs differently. While homogenous selection was the prevailing process controlling assembly of the microbial communities, the neutral processes (e.g., dispersal limitation, drift and others) were more important for the functional genes. This study suggested complexity and dynamics for the subsurface microbiomes, their functionalities and assemblies, even between the niches located in proximity or within the same geological formation. It underscored the significance to include all the geochemical interface components for a more holistic understanding of the biogeochemical processes in subsurface ecosystems.