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Article Processing Charges for This Open-Access Depth, Rendering Deeper and Older OM Bioavailable for Mi- Publication Were Covered by a Research Crobial Decomposition Biogeosciences, 15, 1969–1985, 2018 https://doi.org/10.5194/bg-15-1969-2018 © Author(s) 2018. This work is distributed under the Creative Commons Attribution 3.0 License. Substrate potential of last interglacial to Holocene permafrost organic matter for future microbial greenhouse gas production Janina G. Stapel1, Georg Schwamborn2, Lutz Schirrmeister2, Brian Horsfield1, and Kai Mangelsdorf1 1GFZ, German Research Centre for Geoscience, Helmholtz Centre Potsdam, Organic Geochemistry, Telegrafenberg, 14473 Potsdam, Germany 2Alfred Wegener Institute, Helmholtz Centre for Polar and Marine Research, Department of Periglacial Research, Telegrafenberg, A43, 14473 Potsdam, Germany Correspondence: Kai Mangelsdorf ([email protected]) Received: 14 March 2017 – Discussion started: 17 March 2017 Revised: 2 February 2018 – Accepted: 6 February 2018 – Published: 4 April 2018 Abstract. In this study the organic matter (OM) in sev- 1 Introduction eral permafrost cores from Bol’shoy Lyakhovsky Island in NE Siberia was investigated. In the context of the observed The northern areas of the Eurasian landmass are under- global warming the aim was to evaluate the potential of lain by permafrost, which is defined as ground that remains freeze-locked OM from different depositional ages to act as colder than 0 ◦C for at least 2 consecutive years (Washburn, a substrate provider for microbial production of greenhouse 1980). These areas contain a large reservoir of organic car- gases from thawing permafrost. To assess this potential, the bon freeze-locked in the permafrost deposits (French, 2007; concentrations of free and bound acetate, which form an Zimov et al., 2009). Hugelius et al. (2014) estimated that appropriate substrate for methanogenesis, were determined. about 1300 Pg (1 Pg D 1015 g D 1 Gt) of soil organic carbon The largest free-acetate (in pore water) and bound-acetate is stored in the upper 0–3 m in the northern circumpolar per- (organic-matrix-linked) substrate pools were present in in- mafrost region, which is highly vulnerable to climate warm- terstadial marine isotope stage (MIS) 3 and stadial MIS 4 ing (Grosse et al., 2011; Schmidt et al., 2011; Mu et al., Yedoma permafrost deposits. In contrast, deposits from the 2014). Today, Arctic summer temperatures are higher than last interglacial MIS 5e (Eemian) contained only a small in the past 400 years (Chapin III et al., 2005). Thus, as a pool of substrates. The Holocene (MIS 1) deposits revealed consequence of Northern Hemisphere warming an increase a significant bound-acetate pool, representing a future sub- in ground temperature, changes in soil drainage, deepening strate potential upon release during OM degradation. Addi- of the active layer (seasonally thawed surface layer), spa- tionally, pyrolysis experiments on the OM allocated an in- tial retreat of permafrost, and changes in vegetation have al- creased aliphatic character to the MIS 3 and 4 Late Pleis- ready been reported for the Arctic (Davidson and Janssens, tocene deposits, which might indicate less decomposed and 2006; Anisimov, 2007; Romanovsky et al., 2010; Mueller presumably more easily degradable OM. Biomarkers for past et al., 2015). During permafrost formation low tempera- microbial communities, including those for methanogenic ar- tures, anoxic soil conditions, and low rates of organic mat- chaea, also showed the highest abundance during MIS 3 and ter (OM) decomposition (Schimel and Schaeffer, 2012) re- 4, which indicated OM-stimulated microbial degradation and sult in high rates of OM accumulation (Kuhry et al., 2009; presumably greenhouse gas production during time of de- Zimov et al., 2009; Schirrmeister et al., 2011a). The cur- position. On a broader perspective, Arctic warming will in- rently observed thawing of permafrost promotes the acces- crease and deepen permafrost thaw and favor substrate avail- sibility of accumulated and freeze-locked OM and nutri- ability from older freeze-locked permafrost deposits. Thus, ents for microbial turnover. This results in increased micro- the Yedoma deposits especially showed a high potential for bial activity and, consequently, in increased OM decompo- providing substrates relevant for microbial greenhouse gas sition rates (Dutta et al., 2006; Schmidt et al., 2011). Previ- production. ous studies on permafrost samples from Holocene (marine Published by Copernicus Publications on behalf of the European Geosciences Union. 1970 J. G. Stapel et al.: Substrate potential of last interglacial to Holocene permafrost OM isotope stage (MIS) 1) and Late Pleistocene (LP) Yedoma trations. LMWOAs such as acetate are important and easily deposits, which represent widespread ice-rich paleosol for- convertible substrates for microbial metabolism (Ganzert et mations in NE Siberia, have shown that microbial degrad- al., 2007). Acetate is a well-known substrate for methanogen- ability of the freeze-locked OM seems to depend on the esis (Chin and Conrad, 1995). Thus, acetate concentrations amount and composition of organic carbon rather than on the provide valuable information on the greenhouse gas produc- age of the deposits (Knoblauch et al., 2013; Strauss et al., tion potential of the respective OM (Stapel et al., 2016). On 2015; Stapel et al., 2016). As observed in incubation exper- the one hand, acetate can be dissolved in pore water and iments on permafrost samples of different ages (Waldrop et cryostructures (e.g., segregated ice) of permafrost deposits. al., 2010; Lee et al., 2012; Lipson et al., 2012; Knoblauch et This acetate represents a free-substrate pool, which is di- al., 2013; Schadel et al., 2014; Walz et al., 2017), degrada- rectly bioavailable for microorganisms. On the other hand, tion of this OM can lead to enhanced microbial production acetate can be bound to the organic matrix (e.g., by ester and release of greenhouse gases such as carbon dioxide and linkage) forming a future substrate pool upon liberation via methane to the atmosphere (Wagner et al., 2003; Schuur et geochemical or microbial alteration of the OM (Glombitza et al., 2008; McGuire et al., 2009; Knoblauch et al., 2013). This al., 2009a, b; Stapel et al., 2016). release is expected to have strong feedback on global warm- In addition, microbial biomarkers such as phospholipid ing and with that on further permafrost degradation (Schuur fatty acids (PLFAs) and glycerol dialkyl glycerol tetraethers et al., 2008). Thus, due to the carbon–climate feedback cy- (GDGTs) were analyzed to examine the interaction of cle the permafrost region bears the risk of acting as a self- present and past microbial communities with the OM accu- reinforcing system exacerbating global warming. mulated in the past. Phospholipid esters are essential mem- NE Siberian permafrost formation had already started in brane components of living bacterial cells (Zelles, 1999) and the late Pliocene, e.g., at today’s coasts and islands along are hydrolyzed rapidly after cell death (White et al., 1979; the Dmitry Laptev Strait (Arkhangelov et al., 1996). These Logemann et al., 2011). Therefore, their fatty acid side chain deposits provide a unique paleoenvironmental archive with inventories (PLFAs) are used as an indicator for viable mi- stratigraphic patterns of long-lasting accumulation periods croorganisms in sediments (Haack et al., 1994; Bischoff et of permafrost during glacial periods, as well as permafrost al., 2013). In contrast, biomarkers such as GDGTs and ar- degradation features during interglacial periods (Andreev et chaeol represent membrane lipids of dead microbial biomass al., 2004, 2009; Wetterich et al., 2009, 2011). Permafrost since they are already partly degraded as indicated by the deposits were accumulated under continental cold climate loss of their head groups (Pease et al., 1998). While archaeol conditions, accompanied by syngenetic ice-wedge growth and GDGTs with isoprenoid tetraether bridges (isoGDGTs) (Wetterich et al., 2011) during glacial periods, e.g., the mid- represent archaeal biomass, GDGTs with branched tetraether dle Pleistocene (Saalian) and Late Pleistocene (Weichselian; bridges (brGDGTs) derive from bacteria (Weijers et al., Yedoma deposits) (Andreev et al., 2004; Schirrmeister et al., 2006a, b). However, it should be mentioned that the brGDGT 2013). In contrast, during the Eemian (MIS 5e) and Holocene biomarkers only represent part of the bacterial community interglacial periods, extensive thawing of ice wedges and (Weijers et al., 2006a, b; Schouten et al., 2013), while the ar- permafrost deposits led to the formation of thermokarst de- chaeal markers cover most of the past archaeal community pressions, as well as of thermo-erosional valleys and small (Pancost et al., 2001; Koga and Morii, 2006). In permafrost rivers (Andreev et al., 2004; Ilyashuk et al., 2006; Wetterich regions and peatlands archaeol is used as a biomarker for et al., 2009). According to pollen and insect data, the cli- methanogenic archaea (Bischoff et al., 2013; Pancost et al., mate of the Eemian resulted in an open grass and grass– 2011). sedge tundra similar to the modern situation (Kienast et al., The feedback between climate warming and microbial 2008). The mid-Eemian environment was characterized by greenhouse gas generation from thawing permafrost is a 4–5 ◦C higher summer temperatures than today, with greater topic of large global interest and intensive scientific debate seasonal temperature variations in the Northern Hemisphere (Zimov et al., 2006; Koven et al., 2011; Schuur et al., 2015). (Andreev et al., 2004; Dahl-Jensen
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