Although atmospheric carbon levels are rapidly rising due to anthropogenic fossil greenhouse gas (GHG) emissions5, its reservoir size is dwarfed by carbon stored in the ocean, soils, biosphere, and rocks6. Shales and other sedimentary deposits store around 90% of global organic carbon1. However, this fossil rock-derived or petrogenic organic carbon (OCpetro) has been widely neglected as a potential source for microbially mitigated atmospheric GHGs2. Traditionally, OCpetro has not been included in the active carbon cycle as the majority of it was synthesized, deposited, and degraded millions of years ago and is commonly regarded as non-bioavailable2. However, within the last two decades, several studies have investigated the availability of OCpetro from different sources as a substrate for microbes, painting a more diverse picture of its bioavailability2,7−9. A proper assessment of OCpetro bio-availability and its potential impact on global GHG concentrations becomes increasingly important as more evidence of microbes’ role in releasing GHGs from OCpetro into the atmosphere is discovered10,11.
Previous work focused on dissolved organic carbon (OC) from glacial runoff, showing it to be highly bio-available, despite its old age12,13. Although microbial communities may play a crucial role in glacial nutrient and carbon cycling14,15, the extent to which the particulate OC supplied by glaciers can be utilized by microbes after its redeposition is virtually unexplored. According to conservative estimates, fjords bury about 18 Mt of OC annually (~ 11% of marine carbon burial)4, with an increasing contribution of OCpetro as catchment glaciation increases towards higher latitudes and altitudes16. Globally, about 11% of landmasses are covered by polar ice sheets and alpine glaciers17, eroding into the underlying bedrocks18. Increasing temperatures at high latitudes19 are expected to increase runoff and sediment export from both polar glaciers20,21 and ice-sheets3 to downstream depositional environments, thus increasing OCpetro fluxes in the upcoming decades17,21. At marine-terminating glaciers, the bulk of this OCpetro is deposited within a distance of several kilometers from glacier termini22, with a strong dominance of particulate OC over dissolved OC exported from ice sheets23–25. However, OCpetro deposition is not limited to fjords but may supply 40–50% of OC buried in Arctic Ocean sediments26. The degradation of even a small fraction of this vast pool of additional OCpetro would cause an increase of fossil GHG emissions from marine sediments in the coming decades and potentially create a positive feedback loop of rising temperatures and glacier runoff derived fossil GHG emissions.
To investigate this process, we analyzed three sediment cores, two short and one long, from Hornsund Fjord, Svalbard (Fig. 1). Hornsund’s marine-influenced main basin is separated from the tidewater-glacier dominated inner basin Brepollen, by a shallow sill. The Brepollen basin was formed during the last century following the post Little Ice Age deglaciation27,28. The most marine influenced core (27 cm long core He519_2–3) was retrieved from the center of the main basin at a depth of 202 m. It records the sedimentary history from approximately 1950s to 2018 CE. A gravity core was collected in the Brepollen basin center (149 cm long core HH14-897-GC-MF) at a water depth of 140 m, archiving the time span from 1960s to 2014 CE. The 23 cm long core, He560_26-2-K1, was taken ~ 1 km from the glacier termini at a water depth of 46 m, covering the time period from about 2012 to 2020 CE (details in methods).
Since the late 19th century, the local glaciers have been retreating rapidly at rates of several tens of meters to more than 100 m annually28, simultaneously shifting the sedimentary depocenter alongside the glacier termini position29,30. Sediment accumulation rates in the studied core locations varied from more than 10 cm to a few mm per year with respect to distance from retreating glacier termini. Average total OC contents range between 1.3 ± 0.1 to 1.9 ± 0.1 wt.% and are constant throughout the individual cores independent of glacial proximity (Fig. 2a). The origin of the OC was assessed using several geochemical parameters and biomarker indices including bulk δ13C, fatty acid based terrestrial aquatic ratio (TAR)31, BIT-Index as a soil OC marker32, n-alkane carbon preference index (CPI) as an indicator for degradation/thermal maturity33 (Fig. 2 b-f; details in methods), and bulk radiocarbon (F14C) signature (Fig. 3 Ia, IIa, IIIa). Contributions to the OC pool by terrestrial plants and soils can be neglected based on both the low TAR- ratio and BIT-index. Based on the above mentioned biogeochemical parameters, all three cores show a homogenous OC composition consisting of a mixture of two types of material: 1) young, freshly synthesized, labile marine organic matter (OCmarine) from primary production and 2) old, thermally very mature, supposedly non-bioavailable, OCpetro eroded from organic rich sedimentary rocks in the fjord catchment34. Further evidence for a petrogenic origin of much of the organic matter is provided by the infinite compound-specific radiocarbon ages of long-chain n-alkanes extracted from the central Brepollen core (Table S 1). Even though primary production rates in Hornsund are similar35,36 to other fjord systems with marine-terminating glaciers37,38, the relative abundance of sedimentary OCmarine (fmarine) is rather low and increases with increasing distance to the glacier termini. The fmarine-value was estimated using an isotope mass balance based on F14C of the bulk total organic carbon (TOC), with two endmembers: one modern OCmarine (F14C ~ 1 = modern) and one fossil OCpetro (F14C = 0 = fossil; details in methods). The short core in the vicinity of glacier termini and the long core in the center of the Brepollen basin both have low fmarine-values of 2 ± 2% to 11 ± 2%. By contrast, in the short core (He519_2–3) from the fjord main basin, the fmarine ranges from 42 ± 2% at the core top to 26 ± 6% at the bottom. Overall, the TOC age is primarily controlled by the input of OCmarine as this input is the main difference between the OC deposited in the main basin versus the Brepollen basin.
Due to the characteristic F14C signature of the two pools, we were able to use 14C as an inverse tracer (absence of 14C) under the assumption that the isotopic signature of the substrate (i.e. in sediments) will be passed on through the heterotrophic utilization into the synthesized biomass7. Following the approach of Petsch et al. (2001)7, we assessed the bioavailability of these two OC pools in the sediment cores by radiocarbon analyses of the fatty acid (FA) side chains of intact polar lipids (IPL), extracted with a modified Bligh and Dyer approach39. Bacterial IPLs have been reported to decay within days to weeks after cell lysis and are therefore regarded as indicators for living microbiota40–42. Bacterially produced FAs Cbr−15:0 and C16:1 n−79 were purified into single compound fractions and subsequently radiocarbon dated. With this approach, we were able to identify the average F14C signature of the substrate utilized by bacteria in the sediment9. To ensure bacterial FA origin, precursor lipids were determined by high pressure liquid chromatography coupled to mass spectrometry (HPLC-MS).
Using HPLC-MS, the dated Cbr−15:0 and C16:1 n−7 FAs were found to derive from a diverse group of phospholipid precursors: mainly phosphatidylglycerol and phosphatidylethanolamine in the glacier termini and Brepollen long core and additionally phosphatidylcholine in the main basin core (Figure S 1). While most of these lipids can be assigned to sulfate-reducing bacteria43 or other sedimentary marine bacteria44, minor contributions of potentially algae-derived betaine-lipids and phosphatidylcholine (< 10%) could potentially lead to an increase in the measured F14C FA values and hence an underestimation of OCpetro degradation (details in supplement).
In the marine-influenced main basin core (He519_2–3), compound-specific F14C values for IPL-FAs within the topmost part of the core (< 15 cm; F14C = 0.939 ± 0.008 to 1.002 ± 0.009) agree closely with modeled surface DIC values (F14C = 1.013 ± 0.015 to 1.116 ± 0.020), indicating an exclusive or at least strong preferential utilization of recently synthesized OCmarine (Fig. 3 Ia). Further downcore (17–21 and 21–24 cm), the FAs diverge from modeled DIC signatures toward lower F14C values (F14C < 1.000 ± 0.007), indicating an increase in OCpetro utilization. Interestingly, this shift mirrors with a decrease of fmarine from 30–42% in the topmost 15 cm to less than 30% below. Nevertheless, OCmarine is the primary, but not exclusive substrate utilized by the sedimentary microbiome in sediment core He519_2–3 while an apparent shift towards increasing OCpetro utilization occurs downcore.
A different picture emerges at the glacier termini core (He560_26-2-K1, Fig. 3 IIIa). The C16:1 n−7 F14C values range between 0.767 ± 0.011 and 0.697 ± 0.016, which is far lower and outside the 2σ uncertainty of the modeled surface DIC F14C (ranging between 1.009 ± 0.015 and 1.023 ± 0.015). This indicates the substantial uptake of OCpetro into the bacterial membrane lipids. Unfortunately, sedimentary contents of Cbr−15:0 were too low to perform compound-specific radiocarbon dating. IPL-FA data from the Brepollen long core (HH14-897-GC-MF, Fig. 3 IIa) show F14C values similar to those from the He560 glacier termini core at the topmost interval. As depth increases, the IPL-FA signatures shift toward even lower F14C values reflecting increasing OCpetro utilization in sediments representing depositions closer to the glacier terminis. The values remain rather constant below 30 cm. This shift occurs alongside a decrease in the fmarine in the sediments – similar to the decrease in the main basin core.
The percentage of ancient carbon used for the microbial biosynthesis (Fig. 3 Ib, IIb, IIIb) was estimated with an isotope mass balance model, using a radiocarbon-free, fossil endmember for OCpetro (F14C = 0) and modern OCmarine endmember according to the reservoir age modeled at the respective depth intervals (details in methods). A pronounced difference between the two Brepollen cores to the main basin core is evident from this mass balance estimate. Within the top 15 cm of the main-basin core, ancient carbon accounts for 5 ± 2% to 9 ± 2% of the utilized carbon, whereas in the Brepollen cores, OCpetro contributes up to 37 ± 2% in the topmost intervals. The most proximal core at the glacier termini is characterized by extremely high sedimentation rates, fmarine values consistently below 6 ± 2% throughout the core, and fairly constant OCpetro utilization (24 ± 2% to 32 ± 2%). On the contrary, in both the marine-influenced main basin short core and the central Brepollen basin long core, we can observe an increased utilization of OCpetro with increasing depth and decreasing fmarine. The highest estimate of OCpetro utilization reached 55 ± 6% in the central Brepollen core in the depth interval of 86–89 cm, compared to the lowest OCpetro of only 5 ± 6% in the marine influenced main basin core (see above). Here, we show that even over short distances within one fjord system the microbial utilization of OCpetro can vary widely, suggesting both low and substantial GHG emission potential from increasing glacial erosion.
Although we cannot directly identify the mechanisms for OCpetro utilization, we hypothesize that with decreasing abundance of fresh, labile OCmarine, microbes are forced to utilize OCpetro for their biosynthesis. For example, in the interval with the highest percentage of OCpetro utilized for lipid synthesis (HH14 86-89cm) the mass balance suggests that 55 ± 6% of utilized carbon originates from OCpetro when the abundance of labile OCmarine in the sediment is low (fmarine=5 ± 6%). In the topmost three dated intervals of the main basin core, OCpetro utilization is much lower but still accounts for 5 ± 2% to 9 ± 2% when fmarine is above 30%.
Under the assumption that sedimentary microbes use the same substrate for both their anabolic and catabolic pathways, we estimate that heterotrophic remineralization of OCpetro accounts for between 5 ± 2% to 55 ± 6% of local microbiota’s overall energy consumption. This remineralization leads to the conclusion that CO2 (and CH4) emitted from sediments as metabolic end-products originate in some part from fossil sources, indicating a possible positive feedback with increased mobilization of ancient organic-rich deposits in a warming climate.
Our data indicate that OCpetro is indeed microbially utilized after deposition in Hornsund Fjord. These findings contrast previous work suggesting mobilized OCpetro bypasses the active carbon cycle45. Glaciated fjord ecosystems similar to the Hornsund Fjord with high OC-content bedrock in their drainage areas are fairly widespread and can be found in Svalbard46, Alaska47, Greenland48, Franz-Joseph-Land49, and Antarctica50. These ecosystems may likewise supply suitable substrates for microbial degradation to marine sediments. Microbial OCpetro utilization has also been reported from terrestrial shale7. These findings indicate that OCpetro utilization after erosion and redeposition is likely to occur globally. The resulting fossil GHG emissions and associated positive feedback loops may be substantial – even if only a fraction of the OCpetro becomes re-mineralized after deposition or exposure.
Based on our data, we cannot estimate GHG fluxes resulting from OCpetro utilization in marine sediments. However, considering the size17 of the reservoir and the vulnerability of the glacial ecosystems19, further quantitative research into this topic is necessary. Recent studies of the environment based on both modern glacial sediments51 and paleo CO2 isotopic compositions11 indicate that similar utilization of old, previously “locked up” OC may also occur on shore, indicating a larger geographical scope of OCpetro utilization. Therefore, in order to fully grasp the impact of glacial retreat on global carbon budgets, studying these processes in both marine and terrestrial settings may be needed, given the IPCC projections based on the low emission RCP2.6 scenario predict global glacial mass loss of 18% in 2100 relative to 2015, suggesting long lasting effects even in the event of zero anthropogenic GHG emissions19.