The Genetics, Biochemistry, and Biophysics of Carbon Cycling by Deep Life

Abstract

Much of the microbial life on Earth resides below the surface in the crust (Figure 18.1) (1), either buried in marine sediments (2) and petroleum deposits (3) or entrained in aquifers within oceanic and terrestrial rocks (Figure 18.2) (4–8), fluid inclusions in salt, permafrost, and ice (9–11), as well as hydrothermal and geothermal fluids (12,13). The study of deep subsurface life has defined our understanding of habitability and expanded our knowledge of the mechanisms that enables life to live in these environments (14). While the study of deep life may seem like a philosophical exercise, understanding this enigmatic biosphere has important real-world implications for assessing the safety and feasibility of underground storage of spent nuclear fuel and other toxic compounds, sequestration of atmospheric CO2, or acquisition of fuels such as tar sands, deep subsurface coal beds, methane hydrates, or fracking (3,5,15). Organisms inhabiting subsurface environments likely have been isolated from the surface world for hundreds to millions of years (16). Thus, their metabolic lifestyles may differ substantially from those of surface organisms. Even though subsurface environments are diverse (Chapter 16, this volume), subsurface microbes share common biological challenges such as limitations of energy, resources, and space, as well as extremes of pressure, pH, osmolarity, and temperature (Chapter 17, this volume). On the other hand, subsurface environments offer biological advantages, too: environmental stability, protection from UV irradiation, and oxygen. These unique subsurface conditions lead to communities that are often phylogenetically and functionally diverse, with extremely slow population turnover times (14,17,18) and efficient energy metabolisms (14,19). Increasingly, the roles of viruses and eukaryotes, in addition to bacteria and archaea, are being recognized in the deep subsurface biosphere (20–25). Several barriers hamper the study of life in Earth’s crust, such as sample acquisition and the difficulty of retrieving sterile, unaltered samples that have not been contaminated by drilling fluid. However, an even bigger hurdle is the difficulty of studying the copious subsurface microbes with no cultured representatives (13,26). Their functional potential must be pieced together from direct assessments of biomolecules or biochemical processes in natural samples. However, even subsurface microbes related to laboratory cultures with “known” functions, may not perform those functions in the natural