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Lipids of marine Archaea: Patterns and provenance in the water-column and sediments
Authors:Courtney Turich  Katherine H Freeman  Maureen Conte  Stuart G Wakeham
Institution:a Department of Geosciences, Pennsylvania State University, University Park, PA 16802, USA
b Department of Crop and Soil Sciences, Pennsylvania State University, University Park, PA 16802, USA
c Bermuda Institute for Ocean Sciences, Ferry Reach, St. Georges, GE01 Bermuda, Bermuda
d Department of Biochemistry and Molecular Biology, Michigan State University, East Lansing, MI 48824-1319, USA
e Skidaway Institute of Oceanography, 10 Ocean Science Circle, Savannah, GA 31411, USA
Abstract:We measured archaeal lipid distributions from globally distributed samples of freshwater, marine, and hypersaline suspended particulate matter. Cluster analysis of relative lipid distributions identified four distinct groups, including: (1) marine epipelagic (<100 m) waters, (2) marine mesopelagic (200-1500 m) and upwelling waters, (3) freshwater/estuarine waters, and (4) hypersaline waters. A pronounced difference in lipid composition patterns is the near absence of ring-containing glycerol dialkyl glycerol tetraethers (GDGTs) at high salinity. Different archaeal communities populate marine (mesophilic Crenarchaeota and Euryarchaeota), and hypersaline environments (halophilic Euryarchaeota) and community shifts can regulate differences in lipid patterns between marine and hypersaline waters. We propose that community changes within meosphilic marine Archaea also regulate the lipid patterns distinguishing epipelagic and mesopelagic/upwelling zones. Changes in the relative amounts of crenarchaeol and caldarchaeol and low relative abundances of ringed structures in surface waters differentiate lipids from the epipelagic and mesopelagic/upwelling waters. Patterns of lipids in mesopelagic (and upwelling) waters are similar to those expected of the ammonia-oxidizing Group I Crenarchaeota, with predominance of crenarchaeol and abundant cyclic GDGTs; non-metric multidimensional analysis (NMDS) shows this pattern is associated with high nitrate concentrations. In contrast, limited culture evidence indicates marine Group II Euryarchaeota may be capable of producing mainly caldarchaeol and some, but not all, of the ringed GDGTs and we suggest that these organisms, along with the Crenarchaeota, contribute to lipids in epipelagic marine waters. Calculated TEX86 temperatures in mesopelagic samples (reported here and in published data sets) are always much warmer than measured in situ temperatures. We propose lipids used in the temperature proxy derive from both Euryarchaeaota and Crenarchaeota, and observed values of TEX86 are subject to changes in their ecology as influenced by nutrient fluctuations or other perturbations. Applications of published core-top TEX86-SST correlations require that (1) the surface waters are always composed of similar communities with the same temperature response and (2) that deeper water GDGT production is not transported to the sediments. Our lipid distribution patterns demonstrate both surface-water archaeal community differences (which accompany greater nutrient influxes, shoaling of mesopelagic Crenarchaeota during upwelling periods, and possibly due to an influx of terrestrial Archaea), and changes in organic matter transport through the water column can affect the distribution of lipids recorded in sediments. We therefore suggest that reported temperature shifts in ancient applications indicate TEX86 lipids recorded not only temperature changes, but also changes in archaeal ecology, nutrient concentrations, and possibly oceanographic conditions.
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