Microbial Carbon Assimilation within the Walls of Deep-sea Hydrothermal Vent Chimneys

Abstract

Carbon is one of the most abundant elements on Earth stored in a multitude of reservoirs and constantly cycled through various processes occurring on our planet. Although it represents only a small percentage of the total carbon on Earth, the biosphere is the most active of all carbon reservoirs. We have a comparatively large knowledge of the surface biosphere and primary production associated with phytoplankton and green plants, as well as respiration of organic compounds. A substantial biosphere, driven by "dark energy" or chemical disequilibria may exist for kilometers beneath the continents and the seafloor. Water-rock reactions at high temperatures mobilize the reducing power of the deep Earth, and upon mixing with seawater produce copious and diverse energy sources which can support autotrophic growth. Several remarkable cases of chemotrophic carbon assimilation have been demonstrated since the discovery of the deep-sea vents more than 30 years ago (e.g. bacterial endosymbionts inhabiting the tube worm trophosome), and the isolation of a number of thermophilic and hyperthermophilic chemolithoautotophs. To date, there are six known pathways of carbon assimilation, including the canonical Calvin Benson-Bassham pathway. All of the most recently discovered pathways have been found in thermophiles and Archaea specifically all likely to occurring at deep-sea hydrothermal vents. This study seeks to document the occurrence of autotrophic microorganisms in the context of thermal and chemical gradients within the walls of deep-sea vent chimneys. Furthermore, we show that the phylogeny of genes associated with the Calvin Benson-Bassham cycle is associated with the environmental characteristics in which it occurs. This work has implications for understanding feedbacks between environmental characteristics and carbon assimilation as well as the evolutionary history of carbon fixation pathways. These pathways were likely operative since early in Earth's history, and overlap with conditions which favor the abiotic synthesis of small organic molecules. Research in this realm thus may provide clues to the origins and diversification of carbon fixation pathways as well.