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Marine subsurface hydrocarbon reservoirs and the associated microbial life are among the least characterized ecosystems on Earth. Our understanding of the biological and abiotic processes associated with hydrocarbon production and consumption within these reservoirs is limited by the logistical challenge of obtaining microbial contamination-free samples from these systems. As a result, fundamental questions regarding deep subseafloor hydrocarbon systems have remained unanswered. These include

  • What role does subsurface microbial activity play in the formation of hydrocarbons and hydrocarbon reservoirs?

  • Do deeply buried hydrocarbon reservoirs, such as natural gas deposits and coalbeds, act as geobiological reactors that sustain subsurface life by releasing nutrients and carbon substrates?

  • Do the conversion and transport of hydrocarbons and other reduced compounds influence biomass, diversity, activity, and function of deep subseafloor microbial communities?

  • What are the fluxes of both thermogenically and biologically produced organic compounds, and how important are these for the carbon budgets in the shallower subsurface and overlying ocean?

To address these important scientific questions, Integrated Ocean Drilling Program (IODP) Expedition 337 aimed to drill into deeply buried coalbeds off the Shimokita Peninsula, Japan, in the northwestern Pacific using the riser drilling system of the D/V Chikyu.

The deep subseafloor biosphere

Subseafloor sediments harbor a vast microbial biomass (Parkes et al., 1994, 2000; Whitman et al., 1998; Lipp et al., 2008; Kallmeyer et al., 2012; Hinrichs and Inagaki, 2012). To date, microbial cells have been detected in sediment as old as the Cretaceous and as deep as 1626 meters below seafloor (mbsf) (Newfoundland margin, Ocean Drilling Program [ODP] Leg 210; Roussel et al., 2008). Diagenetic models of pore water chemical constituents and radioactive and stable isotope tracer incubation experiments show that metabolic activities of deep subseafloor microbes are extremely low because of the low supply of nutrient and energy substrates (D’Hondt et al., 2002, 2004). Though recent studies suggest a large fraction of microbial cells to be dormant or endospores (Lomstein et al., 2012; Langerhuus et al., 2012), experiments have demonstrated that most cells restore physiological activity when exposed to energy-replete conditions in the laboratory (Morono et al., 2009). Moreover, past studies have shown the subseafloor microbial activity to be stimulated at geochemical and/or lithologic interfaces such as porous ash layers and sulfate–methane transition (SMT) zones (Inagaki et al., 2003; Parkes et al., 2005; Biddle et al., 2006; Sørensen and Teske, 2006). The metabolic activities of subseafloor microbial communities are largely controlled by the flux of bioavailable electron donors and/or acceptors. These derive either from photosynthetic primary production in overlying seawater or terrestrial environments (D’Hondt et al., 2004, 2009; Lipp et al., 2008) or from fluids entering sedimentary habitat from the underlying Earth’s crust (Cowen et al., 2003; Nakagawa et al., 2006; Engelen et al., 2008; Orcutt et al., 2011). Thus, sedimentological characteristics, such as sediment organic matter content, and lithologic characteristics, which influence fluid flow regimes, determine the energy available to subseafloor life and control habitability of the deep subseafloor environment.

Culture-independent molecular ecological surveys of 16S rRNA gene fragments reveal that microbial communities in continental margin sediment are predominantly composed of species lacking cultivated relatives, such as Bacteria within the candidate division JS1, Chloroflexi, and Planctomycetes, and Archaea within the Deep-Sea Archaeal Group, the Miscellaneous Crenarchaeotal Group, and the South African Gold Mine Euryarchaeotal Group (e.g., Inagaki et al., 2003, 2006b; Inagaki and Nakagawa, 2008). The carbon isotopic analysis of intact polar lipids and fluorescence in situ hybridization (FISH)-stained cells suggest that heterotrophic archaea significantly contribute and sometimes even dominate microbial populations in organic-rich sediment (Lipp et al., 2008; Kubo et al., 2012) or in SMT zones, where the occurrence of anaerobic oxidation of methane (AOM) mediated by methanotrophic archaea and sulfate-reducing bacteria takes place (Biddle et al., 2006). Despite the significance of an organic-fueled microbial ecosystem in biogeochemical cycling within continental margin sediment, the metabolic pathways of organic matter degradation and fluxes of secondary metabolites remain largely unknown (e.g., Hinrichs et al., 2006; Onstott et al., 2010).

Coal diagenesis: microbiological significance for iogeochemical cycles

Within the generally energy-starved deep subseafloor biosphere, deeply buried immature coal (e.g., lignite) is a potential source of nutrients and energy for microbial communities. Previous studies of terrestrial coal deposits suggest that microorganisms play important ecological roles in coal diagenesis, producing substantial quantities of coalbed methane and secondary products (e.g., Brown et al., 1999; Detmers et al., 2001; Shimizu et al., 2007; Krüger et al., 2008; Strapoc et al., 2008; Jones et al., 2008; Fry et al., 2009; Glombitza et al., 2009; Orem et al., 2010; Ünal et al., 2012). The microbial communities in terrestrial coal habitats are phylogenetically diverse, despite often having low cell densities (<106 cells/cm3). Methane-producing archaea (i.e., methanogens) such as the genera Methanoculleus, Methanobacterium, Methanolobus, and Methanosarcina, as well as potential acetate-producing bacteria (i.e., acetogens) such as Acetobacterium, were predominantly detected from a deep borehole aquifer directly connected to the coal deposits in the Hokkaido Island, Japan (Shimizu et al., 2007). Using incubation tracer experiments and FISH, active aceticlastic methanogenesis was found to occur even in a highly altered graphite deposit (Krüger et al., 2008). Fry et al. (2009) reported large cultivable populations of sulfate-reducing bacteria, methanogens, acetogens, and lignite-utilizing heterotrophs in the uplifted coaly sediment of northern New Zealand based on most probable number cultivations. In terrestrial deep subsurface shales, metabolic activities were stimulated at geologic interfaces between coal and sand/silt layers (e.g., Krumholz et al., 1997), and concentrations of organic acids were higher in coal than other layers, consistent with the co-occurrence of coal diagenesis and microbial processes.

Despite the microbiological and (bio)geochemical significance of coaly deposits for the global carbon cycle, there have been no studies of coal layers deeply buried underneath the subseafloor, mainly because of safety regulations applied to hydrocarbon gas–related hazards during riserless drilling. In continental margin sediment, large quantities of gaseous hydrocarbons and their derivatives (e.g., H2 and organic acids) are generated by thermogenic and/or biogenic degradation processes of deeply buried organic matter such as lignite coal. All of these diagenetic compounds are potential nutrient and energy sources to deep subseafloor microbial communities. Hence, microbial activity associated with deeply buried coalbeds may influence characteristics of dissolved gases and organic matter, as well as the accumulation of gas hydrates in shallow sedimentary sequences. The relationship between deep subseafloor hydrocarbon systems and their microbial inhabitants is a frontier research theme in geochemistry and geobiology that can only be better understood through dedicated research initiatives such as Expedition 337.

Exploring the feasibility of CO2 sequestration in deep offshore geological repositories

To date, CO2 capture and sequestration (CCS) into deep subsurface environments, such as oil, gas, and porous aquifers, is considered a potential means to reduce anthropogenic release of CO2 to the atmosphere and weaken the negative impact of anthropogenically induced climate change. CCS offshore in deep subseafloor environments has a number of advantages, including fewer risks than shallow-water CCS (House et al., 2006; Schrag, 2009). It has been predicted that CCS can potentially reduce future world emissions from fuel energy by ~20% (Dooley et al., 2006). In a terrestrial saline aquifer located in Germany, CO2 injection has stimulated microbial growth and activity, indicating that deep microbial communities respond to drastic environmental change (Morozova et al., 2010; Krüger et al., 2011). In deep-sea CO2 seeps, small microbial populations that mediate carbon cycling have been observed in sediment under high CO2 and low pH conditions (Inagaki et al., 2006a; Yanagawa et al., 2013). By contrast, the behavior and stability of CO2 and its geochemical and biological reactions in deep-marine subsurface repositories are still almost completely uncertain (Onstott, 2005; Kirk, 2011).

Using cored samples from Expedition 337, multiple scientific issues regarding geological CO2 sequestration will be addressed through shore-based ex situ experiments. These include

  • How does liquid or supercritical CO2 penetrate into various lithostratigraphic settings?

  • How does CO2 react with minerals, organic matter, and life in the deep subsurface?

  • What are the impacts of long-term CO2 storage on biogeochemical carbon cycling and the subsurface biosphere?

By conducting various multidisciplinary ex situ experiments using cored materials and performing in situ logging characterizations of the deep-riser hole, Expedition 337 will significantly expand our knowledge of the coalbed subseafloor hydrocarbon system, including the physicochemical and biological factors that determine the potential for CO2 sequestration.