Chemolithotrophic and chemoheterotrophic microorganisms in sedimented and rock-hosted hydrothermal systems

Abstract

Deep-sea hydrothermal vent systems are highly productive ecosystems, where reduced energy sources fuel complex communities of microorganisms, invertebrates and vertebrates. Since decades the oxidation of methane, hydrogen and inorganic sulfur compounds has been extensively studied. However, the role of inorganic nitrogen and of organic compounds as energy source has been investigated only scarcely in hydrothermal fluids, in particular at the sea floor, where hydrothermal fluids exit subsurface. The aim of my thesis was to shed light on these under-investigated topics. In my first project I studied nitrification and the involved microbes that are associated with large, nitrate-respiring and sulfur-oxidizing bacteria (SOB) of the genus Beggiatoa. These SOB formed mats and covered sulfide- and ammonia-rich hydrothermal sediments in the Guaymas Basin. In these mats, nitrification rates were measured using 15N-labeled ammonium. With up to 605 Mikromol N l-1 mat d-1 the nitrification rates were the highest measured for a deep-sea ecosystem. Diversity and quantitative PCR of the ammonia monooxygenase subunit A gene (amoA) indicated association of ammonia-oxidizing archaea (AOA) and bacteria (AOB) with Beggiatoa mats. In line with this, single cells of AOB and potentially ammonia-oxidizing thaumarchaotes were attached to narrow Beggiatoa-like filaments. Nitrite oxidizing bacteria were also found. Nitrifying bacteria associated with Beggiatoa mats that respire nitrate to ammonium (DNRA) could display a syntrophic consortium that internally cycle nitrogen and thereby reduce loss of bioavailable nitrogen. However, it is not clear whether large SOB in general respire nitrate also to dinitrogen. Therefore, I analyzed the genetic potential of the large SOB "Candidatus Thiomargarita nelsonii" , a close relative of Beggiatoa. The comparison to four other Beggiatoaceae identified genes for both denitrification and DNRA in "Ca. T. nelsonii" and three other Beggiatoaceae. This indicates that both pathways are widely distributed among large SOB and questions the hypothesis of internal N-cycling in mats of large SOB. In my third project I investigated the microbial consumption of organic compounds that are produced in hydrothermal systems. In particular I studied acetate-assimilating heterotrophic communities in the diffuse fluids (temperature range of 4-72 degree Celsius) of two rock-hosted hydrothermal systems. 16S rRNA gene-based diversity analysis and fluorescence in situ hybridization (FISH) showed that either Gammaproteobacteria or Epsilonproteobacteria rapidly grew during short-term (8-12 h) incubations with 13C-acetate. Single cells of both groups incorporated 13C-acetate as shown by nanoSIMS. Marinobacter spp. and a novel group among the Nautiliales could be heterotrophs in these systems. These are potential r-strategists that quickly respond to the fluctuating availabilities of energy sources in hydrothermal fluids.