The molecular products and biogeochemical significance of lipid photooxidation in West Antarctic surface waters

The seasonal depletion of stratospheric ozone over the Southern Hemisphere allows abnormally high doses of ultraviolet radiation (UVR) to reach surface waters of the West Antarctic Peninsula (WAP) in the austral spring, creating a natural laboratory for the study of lipid photooxidation in the shallow mixed layer of the marginal ice zone. The photooxidation of lipids under such conditions has been identified as a significant source of stress to microorganisms and short-chain fatty acids altered by photochemical processes have been found in both marine aerosols and sinking marine particle material. However, the biogeochemical impact of lipid photooxidation has not been quantitatively compared at ecosystem scale to the many other biological and abiotic processes that can transform particulate organic matter in the surface ocean. We combined results from field experiments with diverse environmental data, including high-resolution, accurate-mass HPLC-ESI-MS analysis of lipid extracts and in situ measurements of ultraviolet irradiance, to address several unresolved questions about lipid photooxidation in the marine environment. In our experiments, we used liposomes—nonliving, cell-like aggregations of lipids—to examine the photolability of various moieties of the intact polar diacylglycerol (IP-DAG) phosphatidylcholine (PC), a structural component of membranes in a broad range of microorganisms. We observed significant rates of photooxidation only when the molecule contained the polyunsaturated fatty acid (PUFA) docosahexaenoic acid (DHA). As the DHA-containing lipid was oxidized, we observed the steady ingrowth of a diversity of oxylipins and oxidized IP-DAG; our results suggest both the intact IP-DAG the degradation products were amenable to heterotrophic assimilation. To complement our experiments, we used an enhanced version of a new lipidomics discovery software package to identify the lipids in water column samples and in several diatom isolates. The galactolipid digalactosyldiacylglycerol (DGDG), the sulfolipid sulfoquinovosyldiacylglycerol (SQDG) and the phospholipids PC and phosphatidylglycerol (PG) accounted for the majority of IP-DAG in the water column particulate (≥0.2 µm) size fraction; between 3.4 and 5.3% of the IP-DAG contained fatty acids that were both highly polyunsaturated (i.e., each containing ≥5 double bonds). Using a broadband apparent quantum yield (AQY) that accounted for direct and Type I (i.e., radical-mediated) photooxidation of PUFA-containing IP-DAG, we estimated that 0.7 ± 0.2 µmol IP-DAG m−2 d−1 (0.5 ± 0.1 mg C m−2 d−1) were oxidized by photochemical processes in the mixed layer. This rate represented 4.4% (range, 3–21%) of the mean bacterial production rate measured in the same waters immediately following the retreat of the sea ice. Because our liposome experiments were not designed to account for oxidation by Type II photosensitized processes that often dominate in marine phytodetritus, our rate estimates may represent a sizeable underestimate of the true rate of lipid photooxidation in the water column. While production of such diverse oxidized lipids and oxylipins has been previously observed in terrestrial plants and mammals in response to biological stressors such as disease, we show here that a similar suite of molecules can be produced via an abiotic process in the environment and that the effect can be commensurate in magnitude with other ecosystem-scale biogeochemical processes

Marine heterotrophic bacteria synthesize non-phosphorus lipids upon phosphorus stress

Aquatic Sciences Meeting, Aquatic Sciences: Global And Regional Perspectives - North Meets South, 22-27 February 2015, Granada, SpainPhosphorus (P) is an essential nutrient for life. The replacement of membrane phospholipids with non-phosphorus lipids constitutes an important strategy to allow growth on phosphate-limited environments. In the ocean, this strategy has been reported in phytoplankton, but not in heterotrophic bacteria. A phospholipase C was recently identified to be required for lipid remodelling in a soil bacterium during P-limitation. In this study we show this enzyme is widespread in bacterial taxa and frequently found in ocean metagenomes. In SAR11 and other proteobacterial isolates, this gene is frequently neighbour to a glycosyltransferase that could be involved in glycolipid biosynthesis. Experiments with marine isolates showed up-regulation of transcription of both the phospholipase C and the glycosyltransferase upon P-starvation. These results suggest that marine heterotrophic bacteria may substitute phospholipids for glycolipids to reduce their P-demand. Lipid measurements in environmental samples confirmed that indeed there is an important enrichment in glycolipids in the heterotrophic bacterial fraction under P-depleted conditions. Hence, lipid remodelling seems to be a widespread mechanism among marine microbes for surviving in the vast oligotrophic areas of the oceanPeer Reviewe