The origin and fate of intact polar lipids in the marine environment

Abstract

A promising method for the identification, characterization and enumeration of microbial communities in the natural environment is the measurement of intact polar lipids (IPLs), the basic building blocks of biomembranes. These complex molecules are ubiquitous in nature and have several characteristics that make them useful as proxies for living microbial cells.Within the large molecular diversity encountered in IPLs, certain types are uniquely synthesized by particular organisms, and these specific IPLs can consequently be used as biomarkers for those source organisms. Furthermore, IPLs are thought to degrade very rapidly upon cell death, meaning they are indicative of living cells and can thus be used for estimates of viable microbial cell numbers or biomass. Finally, microbes can actively remodel the IPL composition of their biomembranes in adaptation to their environment, meaning that information about environmental conditions can potentially be obtained from IPL measurements. The aim of this thesis was to use HPLC/ESI-MS/MS to investigate the origins, dynamics and fate of IPLs in the marine environment and thereby for the first time provide an assessment of their use as a tool in marine environmental microbiology.

A laboratory study of IPL degradation in decaying diatom cultures showed that, while degradation rates were initially high, they slowed progressively over time, and the total IPL pool did not degrade completely. However, field studies of marine surface waters and sediments yielded good correlations between IPL abundances and microbial biomass estimates. It thus seems that in most marine environments the majority of the IPL pool is degraded fairly rapidly, and IPLs can indeed be used as proxies for living microbial cells. Nonetheless, the results do imply that care should be taking in settings where IPL degradation may be impeded, for example in anoxic sediments with a high organic matter content.

A comprehensive analysis of the IPL composition of marine surface waters of the North Sea indicated the presence of a large variety of IPLs, with thousands of different IPL species that could provide potential biomarkers. It was found that the microbial community composition was the dominant factor determining the IPL composition, and little evidence was found for a direct influence of environmental conditions. Unfortunately, it also appears that the most abundant IPLs in the world’s oceans are non-specific, which makes it difficult to target specific microbial groups by general IPL screening. For example, in a spatial survey of the biogeographically diverse North Sea tentative sources for the predominant IPL classes could be identified, but only with poor taxonomic resolution (e.g., small algae, cyanobacteria, diatoms). The same was observed for a time series from the Marsdiep tidal inlet, where the IPL composition of the surface water remained remarkably constant throughout the year, despite major shifts in the phytoplankton community composition.

To bring out the full potential of IPLs as biomarkers in (marine) environmental microbiology, it thus seems necessary to focus on specific IPL biomarkers, rather than general screening, and in the future to apply techniques that yield more structural information, particularly in combination with novel bioinformatics approaches (‘meta-lipidomics’).