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Microbiology of the Continental Subsurface

The terrestrial deep subsurface represents a vast, yet poorly understood environment for microbial life. We investigate the diversity, metabolic potential and activity of microbes and microbial communities below the soil zone. By leveraging high-throughput DNA sequencing and advanced bioinformatics methods, we can reconstruct hundreds to thousands of genomes, providing unprecedented insight into the composition and metabolic potential of these hidden microbial ecosystems.


Our studies target shallow aquifers, groundwater, and deep subsurface environments in order to understand biogeochemical processes. In part, our work leverages underground research laboratories that access sites 100s of meters below ground level. The work has relevance to understanding of evolution, global biogeochemical cycling, and astrobiology. The findings will inform the potential use of the subsurface for underground H2 storage and the geological disposal of high-level radionuclide waste as well as policy development. The research may generate novel enzymes and pathways with biotechnology applications.


Terrestrial Deep Subsurface Biosphere in Japan

We are using genome-resolved metagenomics paired with multi-year geochemical monitoring to study microbial communities in the underground research laboratories at Horonobe and Mizunami field sites. This project is a collaborative effort with Yuki Amano (Japan Atomic Energy Agency) and researchers from Yohey Suzuki's group (University of Tokyo).

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Aquifers and groundwater

Although most research is now conducted at other sites, we still leverage an extensive dataset from an aquifer adjacent to the Colorado River, Rifle, USA to study organisms in the subsurface, usually in conjunction with findings from other sites.  
We are studying cold sulfide-rich springs the discharge deep-subsurface groundwater at Alum Rock Park to understand the intersecting activities of members of microbial communities and to uncover aspects of symbiose​s involving candidate phyla radiation (CPR) bacteria and their hosts, in part drawing on insights from sychrotron-based imaging

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Subsurface Hydrogen Metabolism with Implications for Enhanced Hydrogen Storage

Hydrogen is a ubiquitous molecule in natural systems and a key energy source for microbes across diverse ecosystems. Hydrogenases are enzymes that mediate molecular hydrogen metabolism, conserving energy either by hydrogen consumption coupled to the reduction of electron acceptors or hydrogen production related to balancing the redox potential of the cell. Hydrogenase genes have been recovered from diverse terrestrial and aquatic metagenomes, indicating broad ecological roles.

We are investigating hydrogenase diversity and distribution across microbial lineages in the underexplored deep biosphere. Metagenomic and metatranscriptomic analyses, performed in collaboration with the Greening Lab (Monash University), will be integrated with geochemical and isotopic data to develop a comprehensive model of microbiology under subsurface conditions. This model will contribute to an evaluation of microbial interactions with underground stored hydrogen, which has been proposed as a relevant, large-scale solution to variable and intermittent energy production from renewable sources.

Phylogenetic diversity of [NiFe]-hydrogenases in Japan subsurface metagenomes.

Relevant publications

Matheus Carnevali PB, Schulz F, Castelle CJ, Kantor RS, Shih PM, Sharon I, Santini JM, Olm MR, Amano Y, Thomas BC, Anantharaman K, Burstein D, Becraft ED, Stepanauskas R, Woyke T, Banfield JF. 2019. Hydrogen-based metabolism as an ancestral trait in lineages sibling to the Cyanobacteria. Nature communications, 10, 463.
Probst AJ, Ladd B, Jarett JK, Geller-McGrath DE, Sieber CM, Emerson JB, Anantharaman K, Thomas BC, Malmstrom RR, Stieglmeier M, Klingl A, Woyke T, Ryan MC, Banfield JF. 2018. Differential depth distribution of microbial function and putative symbionts through sediment-hosted aquifers in the deep terrestrial subsurface. Nature Microbiology, 3, 328-336.
Hernsdorf AW, Amano Y, Miyakawa K, Ise K, Suzuki Y, Anantharaman K, Probst A, Burstein D, Thomas BC, Banfield JF. 2017. Potential for microbial H2 and metal transformations associated with novel bacteria and archaea in deep terrestrial subsurface sediments. The ISME journal, 11, 1915-1929.
Anantharaman K, Brown CT, Hug LA, Sharon I, Castelle CJ, Probst AJ, Thomas BC, Singh A, Wilkins MJ, Karaoz U, Brodie EL, Williams KH, Hubbard SS, Banfield JF. 2016. Thousands of microbial genomes shed light on interconnected biogeochemical processes in an aquifer system. Nature communications, 7, 13219.
Wrighton KC, Thomas BC, Sharon I, Miller CS, Castelle CJ, VerBerkmoes NC, Wilkins MJ, Hettich RL, Lipton MS, Williams KH, Long PE, Banfield JF. 2012. Fermentation, hydrogen, and sulfur metabolism in multiple uncultivated bacterial phyla. Science, 337, 1661-1665.

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