Oxygen limitation can trigger the production of branched GDGTs in culture

Abstract

Branched glycerol dialkyl glycerol tetraethers (brGDGTs) are ubiquitous and well preserved sedimentary biomarkers. These compounds serve as important palaeoenvironmental indicators due to strong empirical correlations between brGDGT distributions and temperature and pH in modern environments. However, the mechanistic link between temperature, pH, and brGDGT production has been impossible to ascertain thus far due to the absence of a clear biological source for brGDGTs. Here, we report that oxygen limitation triggers brGDGT production in at least one cultured species of Acidobacteria and confirm for the first time the biosynthesis of three structural varieties of brGDGTs, including an uncharacterised isomer of brGDGT Ic. This discovery helps explain why brGDGT producers have been so difficult to identify and provides a pathway towards uncovering the genetic basis and biological function of brGDGTs, which will lead to a more comprehensive understanding of their palaeoenvironmental significance. If the oxygen effects observed here apply more broadly, the empirical calibrations for brGDGT-based temperature and pH reconstructions may currently be missing the effects of oxygen as a relevant and possibly dominant control in the environmental distributions of brGDGTs.

The production of diverse brGDGTs by an Acidobacterium allows a direct test of temperature and pH controls on their distribution

“…Intriguingly, iso-diabolic acids were absent from the lipid profile of strain Ellin6076. The fractional abundance of brGDGTs in the total lipids of strain Ellin6076 is much higher than that in E. aggregans, whose brGDGTs account for only approximately 3% of total lipids (13).…”

“…However, these observations are inconsistent with the increased production of brGDGTs by E. aggregans under low O2 concentrations (13) and the high abundance of brGDGTs in low oxygen environments (15,18). It is likely that brGDGTs are synthesized by a range of bacteria and/or at least some observations from the environment reflect preservation of brGDGTs in anoxic settings rather than higher production.…”

“…The biological sources of brGDGTs in the environment have puzzled many scientists for more than two decades. Despite substantial effort devoted to solving this conundrum (12,13,16,(18)(19)(20)(26)(27)(28), a bacterial pure culture producing the multiple brGDGTs that have been used to construct paleoclimate has been lacking. Here, we found a bacterial strain Ellin6076 is capable of synthesizing multiple brGDGTs as its major cell membrane lipids.…”

“…This was finally confirmed by the examination of the lipid profiles of more than 40 Acidobacterial strains, revealing their widespread production of the potential building block ( iso -diabolic acid) for brGDGTs, and, most importantly, the positive identification of brGDGT-Ia, a tetramethylated brGDGT, in Edaphobacter aggregans Wbg-1 and Acidobacteriaceae bacteria A2-4c (12, 19, 20). Subsequent work has shown that oxygen limitation can trigger the production of more brGDGT-Ia in E. aggregans (13), likely explaining the long-observed association of brGDGTs with low oxygen conditions. However, the majority of brGDGTs that are used in climate proxies were absent from the lipid profiles of Acidobacteria previously examined in cultures (12, 19, 20).…”

“…In particular, considerable efforts have been devoted to improving our understanding and the accuracy of brGDGT-based temperature or pH proxies (2, 10, 11). However, uncertainties persist, many arising from the fact that the microbial producers of these mysterious lipids in the environment remain incomplete (12, 13). This has prevented an examination of the ecophysiology of these microbes and testing of these proxies under laboratory conditions.…”