Microbial Colonization of Deep-Sea Hydrothermal Vent Chimneys

Abstract

Deep-sea hydrothermal vent chimneys harbor some of the most extreme environments supporting life on Earth. In the absence of sunlight, the microbial communities that colonize these deposits are based on energy harvested by chemolithoautotrophs exploiting the chemical disequilibria created as hydrothermal fluids mix with seawater. Although controversial, several models consider deep-sea vent chimneys as likely habitats for primitive ecosystems that developed during the Archean. The goal of this study was to describe spatial and temporal patterns of microbial colonization in deep-sea vent chimneys emitting high temperature (>300°C) fluids. Microbial community composition and structure were evaluated through analyses of 16S rRNA gene sequences recovered from selected samples. This information was compared to parameters reflecting in situ conditions (temperature, mineralogy, chemistry) in order to highlight the potential links between different environmental factors and microbial communities. A relationship was demonstrated between the depth of microbial colonization and characteristics of thermal gradients in the walls of three chimneys collected at Guaymas Basin. In addition, differences in microbial diversity associated with 4- and 72-day-old deposits formed by the same fluids suggest that internal cycling of locally synthesized organic carbon contributes to promote microbial succession in these environments. Processes controlling this succession were further demonstrated by the identification of a sharp transition in the composition and richness of communities associated with newly formed and mature chimneys of the Juan de Fuca ridge. Finally, patterns of community composition observed in chimneys of the Eastern Lau Spreading Center suggest that differences in hydrothermal fluid chemistry and fluid mixing style has direct effects on microhabitat availability within mature deposits. Combined assessments of 16S rRNA gene diversity and environmental conditions provided new insights into dynamics of microbial colonization in high temperature chimneys. In particular, the deployment of instruments allowing the measurements of in situ conditions within the walls of actively forming deposits constitutes a promising approach to define the parameters that constrain microbial life in these environments. Replicating these studies in various settings will provide a higher resolution understanding of the links between natural phenomena ranging from large-scale geological processes to microscopic interactions at deep-sea hydrothermal vents.