An overview of the occurrence of ether- and ester-linked iso-diabolic acid membrane lipids in microbial cultures of the Acidobacteria: Implications for brGDGT paleoproxies for temperature and pH

Jaap S Sinninghe Damsté,W Irene C Rijpstra,Bärbel U Foesel,Katharina J Huber,Jörg Overmann,Satoshi Nakagawa,Joong Jae Kim,Peter F Dunfield,Svetlana N Dedysh,Laura Villanueva

doi:10.1016/j.orggeochem.2018.07.006

Abstract

13,16-Dimethyl octacosanedioic acid (iso-diabolic acid) is a major membrane-spanning lipid of subdivisions (SDs) 1, 3 and 4 of the Acidobacteria, a highly diverse phylum within the Bacteria. It has been suggested that these lipids are potential building blocks for the orphan bacterial glycerol dialkyl glycerol tetraethers (GDGT) that occur widely in a variety of environmental settings. Here, we expand the knowledge on the occurrence of iso-diabolic acid in Acidobacteria by examining the lipid composition of six strains belonging to SDs 6, 8, 10, and 23 of the Acidobacteria, not previously analyzed for these lipids. In addition, we examined 12 new strains belonging to SDs 1, 3 and 4. Acid hydrolysis of total cell material released iso-diabolic acid in substantial quantities (25–39% of all fatty acids) from the strains of SDs 1 and 3 (except “Candidatus Solibacter usitatus”), and, for the first time, strains of SD 6 (6–25%), but not from SDs 8, 10, and 23. The monoglycerol ether derivative of iso-diabolic acid was only dominantly present in SD 4 strains (17–34%), indicating that the occurrence of ether-bound iso-diabolic acid is mainly restricted to SD 4 species. Methylated iso-diabolic acid derivatives were encountered in SDs 1, 3, 4, and 6, but only SD 4 species produced 5-methyl iso-diabolic acid derivatives, whereas the other SDs formed 6-methyl iso-diabolic acids. This suggests that the position of methylation of iso-diabolic acid may be controlled by the phylogenetic affiliation within the Acidobacteria and thus may not be a direct but an indirect response environmental to environmental conditions as inferred from the bacterial GDGT distributions in soil, peat and rivers.

Highlights

IntroductionUnusual glycerol dialkyl glycerol tetraethers (GDGTs) with nalkyl chains containing 2–4 methyl groups (so-called branched GDGTs; brGDGTs; e.g., structures 1–3 in Fig. 1) were identified
Unusual glycerol dialkyl glycerol tetraethers (GDGTs) with nalkyl chains containing 2–4 methyl groups were identified⇑ Corresponding author at: NIOZ Royal Netherlands Institute for Sea Research, Department of Marine Microbiology and Biogeochemistry, and Utrecht University, PO Box 59, 1790 AB Den Burg, The Netherlands.for the first time in peat by isolation and structure determination by NMR spectroscopy (Sinninghe Damsté et al, 2000)
We identified the elbB – elbE gene cluster, which is presumed to be responsible for ether bond formation in bacteria (Lorenzen et al, 2014), in all available whole genomes and complete metagenomes of SD 4 Acidobacteria, but not in C. thermophilum or any other acidobacterium belonging to other SDs

Summary

Introduction

Unusual glycerol dialkyl glycerol tetraethers (GDGTs) with nalkyl chains containing 2–4 methyl groups (so-called branched GDGTs; brGDGTs; e.g., structures 1–3 in Fig. 1) were identified. ⇑ Corresponding author at: NIOZ Royal Netherlands Institute for Sea Research, Department of Marine Microbiology and Biogeochemistry, and Utrecht University, PO Box 59, 1790 AB Den Burg, The Netherlands. For the first time in peat by isolation and structure determination by NMR spectroscopy (Sinninghe Damsté et al, 2000).

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