Diffused vs. Focused Flow – Metaproteogenomic Insights into Effects of Hydrothermal Fluid Flow on Metal-Sulfide Chimney Colonizing Biofilms

At many sites of hydrothermal discharge in the deep-sea, the deposition of metal sulfides from hydrothermal fluids leads to the formation of geological structures known as hydrothermal chimneys. The mixing of reduced hydrothermal fluids with oxygenated seawater leads to the formation of steep redox gradients within the chimney walls. These gradients facilitate the co-existence of metabolically diverse microorganisms in the narrow habitable zone of hydrothermal chimney walls. However, the overall composition of chimney-associated microbial community is usually of low complexity and represents an environment suitable for metaomic-based studies.

We used metagenomic and metaproteomic tools to compare microbial communities colonizing two metal-sulfide chimneys from the Manus Basin back-arc spreading center in the Bismarck Sea off Papua New Guinea. These chimneys were supplied by the same source hydrothermal fluids, but exhibited different fluid flow regimes. One chimney (RMR5) had a focused venting edifice, while the other (RMR-D) displayed diffuse fluid efflux on its entire outer surface.

Although the microbial diversity of both chimneys is similar and dominated by mesophilic Epsilonproteobacteria, our results indicate a strong structuring effect of hydrothermal fluid flow regime on chimney-associated biofilms. The microbial community composition indicates a homogeneous colonization of the diffuse chimney walls. In contrast, the walls of the focused venting chimney appear to be colonized in layers reflecting different temperature tolerances of the dominant microorganisms. Sulfide-oxidation is likely the key metabolism in both chimneys, which is in line with the high sulfide content of the source hydrothermal fluid. However, preliminary metaproteome analysis indicates high activity of low-abundant methanotrophic Bacteria in the diffuser chimney walls. This finding is particularly interesting in light of the very low methane content of the source hydrothermal fluid. Overall, this study is among the first metaprotoemic investigations of hydrothermal vent associated communities and provides deep insights into the metabolic versatility of hydrothermal chimney colonizing microbes.