Carbon fixation and energy metabolisms of a subseafloor olivine biofilm

Abstract

Earth's largest aquifer ecosystem resides in igneous oceanic crust, where chemosynthesis and water-rock reactions provide the carbon and energy that support an active deep biosphere. The Calvin Cycle is the predominant carbon fixation pathway in cool, oxic, crust; however, the energy and carbon metabolisms in the deep thermal basaltic aquifer are poorly understood. Anaerobic carbon fixation pathways such as the Wood-Ljungdahl pathway, which uses hydrogen (H 2) and CO 2 , may be common in thermal aquifers since water-rock reactions can produce H 2 in hydrothermal environments and bicarbonate is abundant in seawater. To test this, we reconstructed the metabolisms of eleven bacterial and archaeal metagenome-assembled genomes from an olivine biofilm obtained from a Juan de Fuca Ridge basaltic aquifer. We found that the dominant carbon fixation pathway was the Wood-Ljungdahl pathway, which was present in seven of the eight bacterial genomes. Anaerobic respiration appears to be driven by sulfate reduction, and one bacterial genome contained a complete nitrogen fixation pathway. This study reveals the potential pathways for carbon and energy flux in the deep anoxic thermal aquifer ecosystem, and suggests that ancient H 2-based chemolithoautotrophy, which once dominated Earth's early biosphere, may thus remain one of the dominant metabolisms in the suboceanic aquifer today.

Ecology of Subseafloor Crustal Biofilms

“…The driving environmental factors and ecological effects of these differences are unknown. To our knowledge, metagenomic analysis of native subseafloor crustal biofilm communities has not be successful to date, although there are two recent metagenomic assessments of biofilms formed during incubations with subseafloor rocks in vitro (Zhang et al, 2016) and in situ (Smith et al, 2019). These studies suggest potential for carbon fixation by biofilm communities using the Wood-Ljundahl reductive TCA cycle, and also the potential for dissimilatory nitrate reduction.…”

Origin of Short-Chain Organic Acids in Serpentinite Mud Volcanoes of the Mariana Convergent Margin

“…These macrofauna feed on abundant chemotrophic microbiota which are sustained by abiotically produced H 2 , CH 4 , and SCOAs as energy donors and seawater-derived O 2 and sulfate as electron acceptors. It has been suggested that the same abiotically produced compounds might also support microbial communities in the upper mantle and in subseafloor basaltic ocean crust (Früh-Green et al, 2004; Lever et al, 2013; Bach, 2016; Smith et al, 2019).…”

Archaeal Communities in Deep Terrestrial Subsurface Underneath the Deccan Traps, India

“…Archaeal microbiome within the organic carbon lean, basement Archaean granite rocks is distinct and constitute predominantly by acetoclastic methanogens ( Methanomicrobia ), ammonia oxidizing autotrophic archaea (SAGMCG-1, AK59, FHMa11 terrestrial group) and other taxa previously reported from diverse organic carbon deprived, deep crystalline environment with low oxygen (Takai et al, 2001; Kendall and Boone, 2006; Sørensen and Teske, 2006; Schneider et al, 2013; Oren, 2014b; Lauer et al, 2016; Wong et al, 2017; Purkamo et al, 2018; Smith et al, 2019). The presence of acetoclastic methanogenic Methanomicrobia as a dominant archaea in GR could be explained by relative higher concentration of acetate in these rocks, compared to BS (data not shown) as well as a lack of hydrogen generating minerals (e.g., olivine and pyroxene).…”

“…Previous studies have provided valuable information on the distribution and composition of archaea within deep igneous terrestrial subsurfaces and their role in carbon, nitrogen and sulfur geocycling (Offre et al, 2013; Ino et al, 2018). Archaea mediated subsurface H 2 cycling, methanogenesis, anaerobic methane oxidation, iron and sulfur redox transformation, and nitrate reduction are crucial components of subsurface lithoautotrophic microbial ecosystem (SLiME) and/or mixotrophic ecosystems (Stevens and McKinley, 2000; Nealson et al, 2005; Gregory et al, 2019; Smith et al, 2019). Because of their extremophilic nature, significance in different biogeochemical cycles and syntrophic relations with bacterial members, archaea are considered as suitable residents of deep subterranean environments.…”

“…The widespread occurrence of methanogenic and anaerobic methane-oxidizing archaea (ANME); members of more versatile Thermoplasmatales are reported from deep granitic environment of the Witwatersrand deep subsurface, Chelungpu fault, Gifu prefecture, and from Precambrian bedrock fluids in Fennoscandian Shield (Takai et al, 2001; Moser et al, 2005; Gihring et al, 2006; Bomberg et al, 2015; Wu et al, 2015; Ino et al, 2016; Purkamo et al, 2018 and references within). Methanogenesis and methane cycling processes are a major contribution of archaea in deep crystalline rock biosphere, which are considered to be closely interconnected with redox transformation of electron acceptors (nitrate, sulfate, metal oxides, and humics) or electron donors (hydrogen, ammonia, nitrite, and sulfide) (Kietäväinen and Purkamo, 2015; Ino et al, 2018; Smith et al, 2019) and thus play significant roles in overall community function. A few studies have profiled the archaeal diversity in the deep terrestrial biosphere, but their distribution and metabolic significance in biogeochemical cycles within deep subsurface igneous provinces remains poorly explored.…”