Querying Microbial Community Structure and Function in the Shallow Subsurface: Observations from Three North American Cave Systems

Selensky, Matthew James

doi:https://doi.org/10.21985/n2-qghh-2p85

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Querying Microbial Community Structure and Function in the Shallow Subsurface: Observations from Three North American Cave Systems

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Caves are accessible windows into the shallow subsurface, serving as transitional ecosystems between the photosynthesis-dependent surface and the deeper subsurface. Without a source of solar energy to ultimately power carbon (C) fixation (photolithoautotrophy), cave ecosystems are either reliant on surface-derived nutrients, recovering reducing power from the microbial oxidation of redox-sensitive inorganic compounds for C fixation (chemolithoautotrophy), or some combination. Often regarded as detrital, surface-dependent ecosystems with few exceptions, caves are also beginning to be understood as hosts for highly dynamic communities of bacteria and archaea capable of a wide range of biogeochemically relevant metabolisms. As transitional ecosystems between two distinct endmembers, caves represent ideal natural laboratories to query the relationship between microbial community composition and biogeochemical functional potential. Here, we employ diverse methodologies to investigate the microbial community structures and potential metabolisms of three distinct cave systems across different climatic regions of North America: 1) the semi-arid continental lava caves of Lava Beds National Monument (California, United States); 2) the submerged, humid tropical Sistema Sac Actun (Quintana Roo, Mexico); and 3) the enormous, humid subtropical Mammoth Cave (Kentucky, United States). Despite significant differences in host rock lithology and other abiotic factors, communities from each cave system are united by the presence of metabolically flexible microbiota. Lipid-specific stable C isotope analysis suggests that Actinobacteriota in biofilms within lava caves at Lava Beds are abundant and actively fix C in the presence of surface-derived organic C. In the anchialine Sac Actun cave system, a large-scale 16S rRNA gene tag survey demonstrates that metabolically flexible taxa such as Comamonadaceae dominate aquifer communities and co-occur with putatively hydrogen- and methane-oxidizing taxa. Throughout Mammoth Cave, several metagenome-assembled genomes classified as Actinobacteriota demonstrate the capacity for hydrogen, carbon monoxide, and/or thiosulfate oxidation to drive RuBisCO-based chemolithoautotrophy. We also provide novel network analysis software (BNGAL) to aid in the modeling and visualization of microbial niche space from complex taxonomic count data. This work identifies several microbial players involved in the mediation of key biogeochemical cycles in the studied cave systems. Surface-independent metabolisms such as chemolithoautotrophy may be a feature of, rather than an exception to, microbial communities in these shallow subsurface environments.

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