Archaea and bacteria with surprising microdiversity show shifts in dominance over 1,000-year time scales in hydrothermal chimneys

Author Posting. © The Author(s), 2009. This is the author's version of the work. It is posted here by permission of National Academy of Sciences for personal use, not for redistribution. The definitive version was published in Proceedings of the National Academy of Sciences 107 (2010): 1612-1617, doi:10.1073/pnas.0905369107.The Lost City Hydrothermal Field, an ultramafic-hosted system located 15 km west of the Mid-Atlantic Ridge, has experienced at least 30,000 years of hydrothermal activity. Previous studies have shown that its carbonate chimneys form by mixing of ~90ºC, pH 9-11 hydrothermal fluids and cold seawater. Flow of methane and hydrogen-rich hydrothermal fluids in the porous interior chimney walls supports archaeal biofilm communities dominated by a single phylotype of Methanosarcinales. In this study, we have extensively sampled the carbonate-hosted archaeal and bacterial communities by obtaining sequences of >200,000 amplicons of the 16S rRNA V6 region and correlated the results with isotopic (230Th) ages of the chimneys over a 1200 year period. Rare sequences in young chimneys were often more abundant in older chimneys, indicating that members of the rare biosphere can become dominant members of the ecosystem when environmental conditions change. These results suggest that a long history of selection over many cycles of chimney growth has resulted in numerous closely related species at Lost City, each of which is pre-adapted to a particular set of re-occurring environmental conditions. Due to the unique characteristics of the Lost City Hydrothermal Field, these data offer an unprecedented opportunity to study the dynamics of a microbial ecosystem's rare biosphere over a thousand-year time scale.This research was supported by the W.M. Keck Foundation to MLS, the NASA Astrobiology Institute through the Carnegie Institution for Science to JAB and through the MBL to MLS, NSF Grant OCE0137206 and NOAA Ocean Exploration support to DSK, and grants 96-2116-M002-003 and 97-2752-M004-PAE to C.-C. Shen