The effects of metabolism and temperature on carbon isotope composition of lipids in marine bacterium Shewanella piezotolerans W

The carbon isotope composition of lipids has been widely used to decode the biogeochemical cycle and reconstruct paleo-environment and paleo-ecological changes over geologic time. However, up to now, little is known about the controls on the carbon isotope signatures of heterotrophic microbes with ecological functions in the ocean. Here, we investigate the carbon isotope fractionation between fatty acids and carbon sources by a representative marine bacterium Shewanella piezotolerans WP3 growing on different organic substrates, including N-acetyl-D-glucosamine (GlcNac), glucose, acetate, pyruvate, L-alanine, and L-glutamate. The effect of growth temperature on the carbon isotope fractionation is also examined using GlcNac as sole carbon source. Our results show that the carbon isotope fractionations vary obviously between different carbon sources: fatty acids are strongly depleted in ¹³C growing on GlcNac and glucose with abundance-weighted average ¹³C/¹²C fractionations ranging from −7.7 to −3.8‰, slightly depleted in ¹³C on acetate and L-alanine (−0.8 to −0.4‰), and enriched in ¹³C on pyruvate and L-glutamate (0.6–2.1‰). More importantly, we found a considerable variation of fractionations between different growth temperatures with strongly ¹³C-depleted at optimal growth temperature (15–20 °C) with abundance-weighted average ¹³C/¹²C fractionations ranging from −5.2 to −4.8‰ and relatively small fractionations on 4 °C, 10 °C and 25 °C (−2.1 to −3.4‰). We hypothesize that the controls on carbon isotope fractionation are associated with decarboxylation and oxidation-related dehydrogenase complex under different growth temperatures. This study proves that carbon isotope fractionation in heterotrophs is related to which pathway for carbon sources enter into the central metabolism, and may be served as useful “fingerprints” for interpreting carbon isotope signatures in sedimentary lipids, and inferring ecological functions of S. piezotolerans WP3 in certain environments, especially in Fe-reducing oceanic sediments.

The complication of measured carbon isotope fractionations between fatty acids and growth substrate. For each organism, bars represent the range of values for all fatty acids. The vertical line is the average value. Data sources:1 This study; 2-6 other studies.