Deuterium-exchange metabolomics identifies N-methyl lyso phosphatidylethanolamines as abundant lipids in acidophilic mixed microbial communities

Abstract

Natural microbial communities are extremely diverse and contain uncharacterized but functionally important small molecules. By coupling a deuterium (D) labeling technique to high mass accuracy untargeted liquid chromatography-electrospray ionization-mass spectrometry (LC-ESI-MS) metabolomic analysis, we found that natural acidophilic microbial biofilms dominated by bacteria of the genus Leptospirillum contained unusual lyso phosphatidylethanolamine (PE) lipids in high abundance (more than 10 nmol/mg of dry biomass). The unusual polar head group structure of these lipids is similar to lipids found in phylogenetically unrelated acidophilic chemoautolithotrophs and may be related to the affinity of these lipids for iron and calcium ions. Correlations of lyso phospholipid and proteome abundance patterns suggest a link between the lyso phospholipids and the UBA-type substrain of Leptospirillum group II. By combining untargeted metabolomics with D exchange we demonstrate the ability to identify cryptic but biologically functional small molecules in mixed microbial communities.

Metabolites Associated with Adaptation of Microorganisms to an Acidophilic, Metal-Rich Environment Identified by Stable-Isotope-Enabled Metabolomics

“…Unusual lyso phosphatidylethanolamine lipids and methylated derivatives previously identified in the Richmond Mine (28) were also found in the mine and bioreactor biofilms presented here. Fischer et al (28) suggested a link between these lipids and the Leptospirillum group II UBA genotype based on correlations of lipid and proteome abundance patterns.…”

“…Unusual lyso phosphatidylethanolamine lipids and methylated derivatives previously identified in the Richmond Mine (28) were also found in the mine and bioreactor biofilms presented here. Fischer et al (28) suggested a link between these lipids and the Leptospirillum group II UBA genotype based on correlations of lipid and proteome abundance patterns. Interestingly, we found features consistent with some of these same lipids (same m/z and retention times for 454.294 and 480.309) in pure cultures of Acidomyces richmondensis , a fungus known to be abundant in the mine and often the dominant eukaryal species (29, 30).…”

“…Together, these results show that fungi and bacteria may both be involved in the metabolism of these lipids. Fischer et al (28) suggested that these lipids may prevent uptake of toxic levels of iron cations in AMD biofilms.…”

Omics on bioleaching: current and future impacts

“…Of the metabolites identified, three are likely to be significant in biofilms: phosphatidylethanolamine lipids, taurine, and hydroxyectoine. The phosphatidylethanolamine lipids detected had been reported in previous studies of acidophilic microbial communities (Fischer et al 2012 ) and were associated with Leptospirillum group II based on correlations of lipid and protein abundance. An interesting role has been suggested by this type of molecule in the biofilm: to be involved in a potential mechanism of resistance to toxic elements present in AMD solutions with a similar composition that the ones found under industrial bioleaching conditions (Druschel et al 2004 ).…”

A biomolecular isolation framework for eco-systems biology

“…Beyond isolated biomolecular characterization, integrated omics combined with relevant statistical analyses offer the ability to unravel fundamental ecological and evolutionary relationships, which are indiscernible from isolated omic data sets (Wilmes et al , 2010). Furthermore, space- and time-resolved integrated omics have the potential to uncover associations between distinct biomolecules, which allows for discovery of previously unknown biochemical traits of specific microbial community members (Fischer et al , 2011). Such linkages will, however, only be discernible if representative biomolecular fractions are obtained.…”