Mono- and Dialkyl Glycerol Ether Lipids in Anaerobic Bacteria: Biosynthetic Insights from the Mesophilic Sulfate Reducer Desulfatibacillum alkenivorans PF2803 ^T

Abstract

bBacterial glycerol ether lipids (alkylglycerols) have received increasing attention during the last decades, notably due to their potential role in cell resistance or adaptation to adverse environmental conditions. Major uncertainties remain, however, regarding the origin, biosynthesis, and modes of formation of these uncommon bacterial lipids. We report here the preponderance of monoalkyl-and dialkylglycerols (1-O-alkyl-, 2-O-alkyl-, and 1,2-O-dialkylglycerols) among the hydrolyzed lipids of the marine mesophilic sulfate-reducing proteobacterium Desulfatibacillum alkenivorans PF2803 T grown on n-alkenes (pentadec-1-ene or hexadec-1-ene) as the sole carbon and energy source. Alkylglycerols account for one-third to two-thirds of the total cellular lipids (alkylglycerols plus acylglycerols), depending on the growth substrate, with dialkylglycerols contributing to one-fifth to two-fifths of the total ether lipids. The carbon chain distribution of the lipids of D. alkenivorans also depends on that of the substrate, but the chain length and methyl-branching patterns of fatty acids and monoalkyl-and dialkylglycerols are systematically congruent, supporting the idea of a biosynthetic link between the three classes of compounds. Vinyl ethers (1-alken-1=-yl-glycerols, known as plasmalogens) are not detected among the lipids of strain PF2803 T . Cultures grown on different (per)deuterated n-alkene, n-alkanol, and n-fatty acid substrates further demonstrate that saturated alkylglycerols are not formed via the reduction of hypothetic alken-1=-yl intermediates. Our results support an unprecedented biosynthetic pathway to monoalkyl/monoacyl-and dialkylglycerols in anaerobic bacteria and suggest that n-alkyl compounds present in the environment can serve as the substrates for supplying the building blocks of ether phospholipids of heterotrophic bacteria.

Biogeochemistry of intertidal microbial mats from Qatar: New insights from organic matter characterisation

“…Nonisoprenoid DAGEs have been detected in hydrothermal environments Jahnke et al, 2001;Pancost et al, 2005Pancost et al, , 2006Bradley et al, 2009;Kaur et al, 2011;Hamilton-Brehm et al, 2013), upper Pliocene iron sulphide nodules (van Dongen et al, 2007), and diverse marine sediments (Hinrichs et al, 2000;Pancost et al, 2001;Blumenberg et al, 2004;Arning et al, 2008;Hernandez-Sanchez et al, 2014). Here, given that the peak concentration of DAGEs corresponded to the presence of sulphate-reducing bacteria, we suggest that these are the source, as has been inferred in settings dominated by anaerobic oxidation of methane (Hinrichs et al, 2000;Pancost et al, 2001;Blumenberg et al, 2004), and consistent with their recent identification in a mesophilic strain of Deltaproteobacteria (Grossi et al, 2015, Vinçon-Laugier et al, 2016.…”

Identification of Ethyl and t-Butyl Glyceryl Ethers Using Gas Chromatography Coupled with Mass Spectrometry

“…It is important to highlight that the characterization of alkylglycerols has received increasing attention in other science areas, [20][21][22] since some of these ethers are considered important biological markers with a role in cell resistance and adaptation. So, considerable efforts have been made to identify them based on their mass spectra.…”

Constraining the formation of authigenic carbonates in a seepage‐affected cold‐water coral mound by lipid biomarkers

“…Additionally, no biomarkers characteristic for AOM have been found in Ca‐excess dolomite‐rich layers (from 150 to 360 cm depth). However, elevated DAGE contents (167 and 265 cm depths; Figure ) points to a link with organoclastic sulphate reduction (see Grossi et al, ). Evidence for pronounced organoclastic sulphate reduction has been observed in Alpha Mound sediments before (Rejas et al, ; Templer et al, ; Wehrmann et al, ), rendering it likely that this process plays a role in Ca‐excess dolomite formation due to an increase of alkalinity induced by this process (Wehrmann, Titschack, Böttcher, & Ferdelman, ).…”

“…High GDGT-0/crenarchaeol and GDGT-2/crenarchaeol ratios observed at 485 cm depth were accompanied by relatively high amounts of DAGEs with two anteiso-C 15 /anteiso-C 15 alkyl chains ( Figure 4b) and a δ 13 C value of − 82‰ ( (Grossi et al, 2015;Vinçon-Laugier, Grossi, Pacton, Escarguel, & Cravo-Laureau, 2016). Despite the uncertainty about the role of DAGE producers at methane seeps, their strong 13 C depletion confirms at least a close relationship to the AOM consortium (Blumenberg et al, 2004;Cook, Keigwin, Birgel, & Hinrichs, 2011;Elvert, Hopmans, Treude, Boetius, & Suess, 2005;Stadnitskaia et al, 2008;Teske et al, 2002).…”

“…DAGEs have commonly been interpreted as biomarkers of the sulphate‐reducing bacteria associated with ANMEs (Hinrichs et al, ; Pancost, Bouloubassi, Aloisi, Sinninghe Damsté, & Shipboard Scientific Party, ), but this inference has never been substantiated. DAGEs have not been found in enrichment cultures of sulphate‐reducing bacteria of AOM consortia (Boetius et al, ; Orphan, Hinrichs, et al, ; Orphan, House, Hinrichs, McKeegan, & DeLong, ), but are common in other, chiefly hydrocarbon‐degrading sulphate‐reducing bacteria (Grossi et al, ; Vinçon‐Laugier, Grossi, Pacton, Escarguel, & Cravo‐Laureau, ). Despite the uncertainty about the role of DAGE producers at methane seeps, their strong 13 C depletion confirms at least a close relationship to the AOM consortium (Blumenberg et al, ; Cook, Keigwin, Birgel, & Hinrichs, ; Elvert, Hopmans, Treude, Boetius, & Suess, ; Stadnitskaia et al, ; Teske et al, ).…”