Molecular studies of the sources and significance of archaeal lipids in the oceans

Abstract

Marine archaea are ubiquitous and abundant in the modem oceans and have a geologic record extending >100 million years. However, factors influencing the populations of the major clades - chemolithoautotrophic Marine Group I Thaumarchaeota (MG-I) and heterotrophic Marine Group II Euryarchaeota (MG-II) - and their membrane lipid signatures are not well understood. Here, I paired techniques of organic geochemistry and molecular biology to explore the sources and significance of archaeal tetraether lipids in the marine water column. Using metagenomics, 16S rDNA pyrosequencing, QPCR and mass spectrometric analyses, I found that uncultivated MG-IL Euryarchaeota synthesize glycerol dialkyl glycerol tetraether (GDGT) lipids - including crenarchaeol, previously thought limited to autotrophic Thaumarchaeota. This finding has important implications for paleoenvironmental proxies reliant upon GDGTs. To investigate the effects of organic matter and bicarbonate + ammonia amendments on archaeal tetraether lipids and microbial community composition, I conducted large scale microcosm experiments. Experimental conditions did not promote the overall growth of archaea, but several changes in tetraether lipid abundance and relative ring distribution suggest that future incubation labeling studies using whole seawater may be valuable in probing the metabolism of individual archaeal clades in mixed populations. A rapid decrease in GDGT concentrations was observed within the first 44 h of the experiment, suggesting that the residence time of these compounds in the open ocean may be short. Changes in functional gene representation and microbial community composition over the course of the experiment provide potential insight into mechanisms of copiotrophy and the identity of bacteria that may degrade GDGTs. Finally, I present the results of a study of the sources and patterns of bacterial and archaeal GDGTs detected in the Lost City Hydrothermal Vent Field. Branched GDGTs, generally considered markers of terrestrial input to marine sediments, were detected in carbonate chimneys of this alkaline site near the mid-Atlantic Ridge. A relatively uncommon H-shaped GDGT was also present, and appears to be a marker of hydrothermal archaeal input rather than a mesophilic euryarchaeotal signal. Taken together, the work presented in this thesis emphasizes the necessity of understanding the biological underpinnings of archaeal lipids in the environment, increasingly used as biomarkers in microbial ecology and paleoenvironmental reconstruction.