Biomarker 14C evidence for sources and recycling of pre-aged organic carbon in Arctic permafrost regions

Permafrost thaw has the potential to release ancient particulate and dissolved organic matter that had been stored for thousands of years. Previous studies have shown that dissolved organic matter from permafrost is very labile and can be used by heterotrophic microbes close to the thaw area. However, it is unknown if ancient particulate organic matter can also be utilized. This study aims to investigate whether arctic microbial communities (bacteria and Archaea) incorporate ancient organic matter potentially released from thawing permafrost into their biomass. We compare and contrast the radiocarbon signatures of microbial lipids and higher plant biomarkers (representing terrestrial organic matter) from five soil profiles and seven deltaic lake sediment cores from the Mackenzie River drainage basin, Arctic Canada. In the surface soils, modern to post-modern short-chain fatty acids (SCFA) ages indicate in situ microbial production, with differential rates of organic carbon (OC) cycling depending on soil moisture. In contrast, SCFA in deeper soils display millennial ages, which likely represent the microbial necromass preserved through mineral association. In deltaic lakes that are disconnected from the river, generally old SCFA suggests the uptake of pre-aged OC by bacteria. In perennially connected lakes, pre-aged SCFA could originate from in situ microbial uptake of old OC or from the Mackenzie River. Higher plant-derived long-chain fatty acids (LCFA) present older radiocarbon ages, reflecting mineral stabilization during either pre-aging in soils (for high closure lakes) or riverine transport (for no and low closure lakes). Archaeal lipids are younger than SCFA and LCFA in high closure lakes, and older in low and no closure lakes, mirroring bulk radiocarbon signatures due to their heterotrophic production. These radiocarbon signatures of bacterial biomarker lipids may therefore reflect microbial incorporation of ancient OC (e.g., derived from permafrost thaw) or exceptional preservation (e.g., through mineral stabilization). Hence, even in relatively high OC environments such as arctic aquatic ecosystems, microbes can rely on ancient OC for their growth.