Geochemical-dependent stratification of microbial chemolithoautotrophy in a high carbon dioxide subsurface aquifer
Final Report Abstract
Subsurface microbial life, which must exist without sunlight, a major energy source on our planet, has been shown to comprise a substantial diversity dominated mainly by yet-to-be cultivated bacteria and archaea. In recent years, we have started to explore this diversity of microorganisms and their genetic machineries using approaches of environmental genomics. However, the distribution of these microorganisms across subsurface ecosystems and their interaction with biotic and abiotic factors remains little understood. In this project, we explored the microbial diversity and its distribution in the geochemically stratified, cold Crystal Geyser (Utah, US), which is driven via high CO2 eruptions from the subsurface. Our hydrogeological investigations revealed that the geyser sources CO2-saturated groundwater from at least three different aquifers of different depth along the Colorado Plateau, which are separated by units of low permeability but transected through the 800-m deep borehole of the geyser. Throughout the geyser’s eruption cycle, which lasted nearly five days, the subsurface fluids sampled at different time points were dominated by groundwater from different depth enabling microbial source tracking based on sampling time. Using genome-resolved metagenomics and singlecell genomics, we reconstructed high-quality genomes of 505 different microbial organisms, 289 of which could be assigned to groundwater of different depths, whereas uncultivated archaea and putative symbionts were partitioned to the deep subsurface. A single organism of the genus Sulfurimonas dominated the groundwater of the shallow subsurface aquifer, likely via nitrogen and carbon fixation, which was encoded in its genome. Metabolic reconstruction of the all organisms’ biosynthetic pathways demonstrated a stratification thereof along the transect of the Colorado Plateau. Three different carbon fixation pathways, the Wood-Ljungdahl pathway, the Calvin Benson Bassham Cycle and the reverse TCA cycle, dominated groundwater from different depths (listed in their dominance from deep to shallow groundwater). Organisms of the bacterial candidate phyla radiation (CPR) and of the archaeal DPANN radiation were mostly prominent in groundwater from the deep subsurface. Investigation of cocorrelation patterns revealed a potential symbiotic relationship between the most dominant archaeon in the ecosystem (Candidatus “Altiarchaeum sp.”, a primary producer) and a putative parasite named Candidatus “Huberarchaeum crystalense” incapable of synthesizing many essential biomolecules like nucleotides. Reconstruction of another complete genome of the DPANN radiation revealed high genome fluidity in the environment for this organism, likely via transposons propagation and homologous recombination, which has not been reported before for this clade of archaea. CPR were the most diverse organisms in all ecosystems accessible through Crystal Geyser. Although these organisms were depleted in CRISPR Cas9 viral defense systems, some surprisingly carried novel CRISPR systems (termed Cas-Y), which are more streamlined than previously known CIRSPR systems. Throughout this project, we deciphered the metabolic and phylogenetic diversity of three different subsurface communities accessible through Crystal Geyser. The results displayed a stratification of microbial diversity and function along the transect of the Colorado Plateau, with putative symbionts partitioned to the deeper subsurface. Investigation of the genomic architecture of putative symbionts revealed that recombination events of these organisms exist in(situ and novel viral defense systems can be explored in yet-to-be cultivated organisms. High CO2 environments - like Crystal Geyser investigated herein -house a tremendous array of microorganisms, all adapted to these extreme CO2 concentrations and bearing a great potential for future biotechnological application in human health and climate change research.
Publications
- (2016). Genomic resolution of a cold subsurface aquifer community provides metabolic insights for novel microbes adapted to high CO2 concentrations. Env Microbiol, 459-474, Vol. 19(2)
Probst AJ, Castelle C, Singh A, Brown CT, Anantharaman K, Sharon I, Hug LA, Emerson JB, Thomas BC, and Banfield JF
(See online at https://doi.org/10.1111/1462-2920.13362) - (2017). New CRISPR-Cas systems from uncultivated microbes. Nature, 237-241, Vol. 524(7640)
Burstein D, Harrington LB, Strutt SC, Probst AT, Anantharaman K, Thomas BC, Doudna JA, and Banfield JB
(See online at https://doi.org/10.1038/nature21059) - (2017). Recovery of genomes from metagenoms via a dereplication aggregation and scoring strategy
Sieber CMK, Probst AJ, Sharon I, Sharrar A, Thomas BC, Hess M, Tringe SG, and Banfield JB
(See online at https://doi.org/10.1038/s41564-018-0171-1) - (2017). Differential depth-based distribution of microbial function and novel symbionts through sediment-hosted aquifers in the deep terrestrial subsurface. Nature Microbiology, accepted
Probst AJ, Ladd B, Jarett JK, Geller-McGrath DE, Sieber CMK, Emerson JB, Anantharaman K, Thomas BC, Malmstrom RR, Stieglmeier M, Klingl A, Woyke T, Ryan MC, and Banfield JF
(See online at https://doi.org/10.1038/s41564-017-0098-y)
