Abstract
Thermophilic methanogens are common autotrophs at hydrothermal vents, but their growth constraints and dependence on H2 syntrophy in situ are poorly understood. Between 2012 and 2015, methanogens and H2-producing heterotrophs were detected by growth at 80°C and 55°C at most diffuse (7–40°C) hydrothermal vent sites at Axial Seamount. Microcosm incubations of diffuse hydrothermal fluids at 80°C and 55°C demonstrated that growth of thermophilic and hyperthermophilic methanogens is primarily limited by H2 availability. Amendment of microcosms with NH4+ generally had no effect on CH4 production. However, annual variations in abundance and CH4 production were observed in relation to the eruption cycle of the seamount. Microcosm incubations of hydrothermal fluids at 80°C and 55°C supplemented with tryptone and no added H2 showed CH4 production indicating the capacity in situ for methanogenic H2 syntrophy. 16S rRNA genes were found in 80°C microcosms from H2-producing archaea and H2-consuming methanogens, but not for any bacteria. In 55°C microcosms, sequences were found from H2-producing bacteria and H2-consuming methanogens and sulfate-reducing bacteria. A co-culture of representative organisms showed that Thermococcus paralvinellae supported the syntrophic growth of Methanocaldococcus bathoardescens at 82°C and Methanothermococcus sp. strain BW11 at 60°C. The results demonstrate that modeling of subseafloor methanogenesis should focus primarily on H2 availability and temperature, and that thermophilic H2 syntrophy can support methanogenesis within natural microbial assemblages and may be an important energy source for thermophilic autotrophs in marine geothermal environments.
Highlights
1 Gt of CH4 is formed globally per year from H2, CO2 and acetate through methanogenesis, largely by methanogens growing in syntrophic association with anaerobic microbes that hydrolyze and ferment biopolymers (Thauer et al, 2008)
Thermophilic methanogens are consistently found in hydrothermal fluids at Axial Seamount, an active deep-sea volcano in the northeastern Pacific Ocean, and most belong to the genera Methanocaldococcus, Methanothermococcus, and Methanococcus (Huber et al, 2002; Ver Eecke et al, 2012; Meyer et al, 2013; Fortunato and Huber, 2016)
The purpose of this study was to determine, among natural assemblages of thermophilic and hyperthermophilic methanogens, if methanogenesis at hydrothermal vents is limited primarily by the availability of H2; if methanogenesis is stimulated by the addition of NH4+; and if H2 syntrophy occurs when natural assemblages of thermophiles and hyperthermophiles are provided only with organic compounds as an energy source
Summary
1 Gt of CH4 is formed globally per year from H2, CO2 and acetate through methanogenesis, largely by methanogens growing in syntrophic association with anaerobic microbes that hydrolyze and ferment biopolymers (Thauer et al, 2008). H2 Limitation and Syntrophy among Vent Thermophiles hydrothermal fluids are high, but are scarce in low H2 environments, as measured by culture-dependent techniques (Stewart et al, 2016), culture-independent techniques (Perner et al, 2007; Flores et al, 2011), and both techniques in tandem (Takai et al, 2004, 2008, 2009; Nakagawa et al, 2005, 2006; Ver Eecke et al, 2012; Lin et al, 2016). This enables sulfate reducers to inhibit methanogen growth by lowering the partial pressure of H2 to concentrations below levels that methanogens can use for growth
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