Sun beams reaching the surface of Earth not only warm our planet but also provide ample energy to living organisms. Photosynthetic organisms capture efficiently the light energy to fix carbon and grow, which feed the rest of the food web such as animals, birds and heterotrophic bacteria. In the deep subsurface, separated from the photosphere by kilometers of rock, chemolithotrophic microorganisms mine energy from geologically produced minerals and gases, a far more difficult existence compared to their photosynthetic comrades on the surface.
Driven by curiosity about what organisms colonize the deep subsurface and how they survive independently from sunlight for at least tens of thousands of years, an international team of scientists from the United States, South Africa and Canada led by Princeton University traveled to 1.3-kilometer underground at Beatrix gold mine in South Africa. The team rode in the “cage” (aka the elevator) together with approximately 100 miners at the dawn, which descends to a depth equivalent to three Empire State Buildings in just several minutes. The team was then guided to the study site that is more than one kilometer away. They walked in a single profile of halogen headlamps turning down one corridor after another winding their way through this completely dark, underground maze. Upon arrival at the borehole, the team unloaded the stainless-steel sampling apparatuses and tens of empty glass and plastic bottles from their 60-70 L backpacks and began an approximately three hours of intense effort to fill up every bottle with pristine underground water and dissolved gas, and set up filtration devices to collect microbial cells. Carrying twice the weight they bore walking in, the team trudged back in silence through the heat and stench pondering what they had seen and looking forward to returning to the surface and analyzing their precious cargo.
Previous studies done by Prof. Tullis C. Onstott (Ph.D. ’81)’s lab at Department of Geosciences have revealed the presence of diverse subsurface microorganisms and geochemical signatures of microbial activities such as methanogenesis, anaerobic methane oxidation, sulfate reduction and denitrification. The study recently published in the Proceedings of the National Academy of Sciences further the work by portraying the microbial processes that actively take place. “We catalog the expression profiles of RNA and protein because these molecules are rather short-lived and therefore they give a strong indication of microorganisms’ recent activities,” said Maggie Lau, the lead author.
The authors laid out the comprehensive network of metabolic pathways, or the metabolic landscape termed by the authors, and revealed that the active microbial processes are more diverse than previously thought. It has been commonly understood that hydrogen is the major fuel in the deep subsurface. Previous investigations have been focusing on studying methanogens and sulfate-reducing bacteria that utilize hydrogen. Strikingly, Maggie Lau and co-workers found that autotrophic sulfur-oxidizing denitrifiers were the most dominant microbial taxa in the studied oligotrophic water, despite the low standing concentrations of reduced sulfur and nitrate. Geochemical models explained that the redox couple of sulfur oxidation and nitrate reduction was energetically more favorable under the native subsurface condition when compared to sulfate reduction. Likewise, anaerobic methane oxidation was energetically more favorable than methanogenesis. These two pairs of microorganisms recycle their metabolic products and form a tight partnership. For example, sulfate-reducing bacteria produce reduced sulfur from sulfate but with diminishing returns in energy as sulfide builds up in the water. The rate of energy yield, however, is increased by the removal of reduced sulfur by sulfur-oxidizing bacteria. Meanwhile, sulfur-oxidizing bacteria rely on the sulfate-reducing bacteria for reduced sulfur, which is converted to sulfate closing the reaction cycle. As a result, by establishing a syntrophic relationship the sulfate-reducing and sulfur-oxidizing bacteria overcome the challenges faced when extracting the limited energy originated from rocks.
This documentation of diverse metabolic reactions and the close metabolic interactions among deep subsurface microorganisms provide new insights in how deep subsurface ecosystems function. The results also demonstrate the amazing power of life and teamwork to cope with unfavorable environment.
Lau MCY, Kieft TL, Kuloyo O, Linage-Alvarez B, van Heerden E, Lindsay MR, Magnabosco C, Wang W, Wiggins JB, Guo L, Perlman DH, Kyin S, Shwe HH, Harris RL, Oh Y, Yi MJ, Purtschert R, Slater GF, Ono S, Wei S, Li L, Sherwood Lollar B, Onstott TC (2016) An oligotrophic deep-subsurface community dependent on syntrophy is dominated by sulfur-driven autotrophic denitrifiers. Proceedings of the National Academy of Sciences doi: 10.1073/pnas.1612244113