Biogeosciences, 13, 283–299, 2016 www.biogeosciences.net/13/283/2016/ doi:10.5194/bg-13-283-2016 © Author(s) 2016. CC Attribution 3.0 License. Microbial methanogenesis in the sulfate-reducing zone of surface sediments traversing the Peruvian margin J. Maltby1, S. Sommer1, A. W. Dale1, and T. Treude1,2 1GEOMAR Helmholtz Centre for Ocean Research Kiel, Department of Marine Biogeochemistry, Wischhofstr. 1–3, 24148 Kiel, Germany 2present address: Department of Earth, Planetary and Space Sciences & Atmospheric and Oceanic Sciences, University of California, Los Angeles (UCLA), CA, USA Correspondence to: J. Maltby ([email protected]) and T. Treude ([email protected]) Received: 7 August 2015 – Published in Biogeosciences Discuss.: 9 September 2015 Revised: 10 December 2015 – Accepted: 21 December 2015 – Published: 15 January 2016 Abstract. We studied the concurrence of methanogenesis tion of hydrogenotrophic activity in the sulfate-depleted zone and sulfate reduction in surface sediments (0–25 cm below at the shallow shelf station (70 m). sea floor) at six stations (70, 145, 253, 407, 990 and 1024 m) Surface methanogenesis appeared to be correlated to the along the Peruvian margin (12◦ S). This oceanographic re- availability of labile organic matter (C = N ratio) and organic gion is characterized by high carbon export to the seafloor carbon degradation (DIC production), both of which sup- creating an extensive oxygen minimum zone (OMZ) on the port the supply of methanogenic substrates. A negative cor- shelf, both factors that could favor surface methanogenesis. relation between methanogenesis rates and dissolved oxy- Sediments sampled along the depth transect traversed areas gen in the bottom-near water was not obvious; however, of anoxic and oxic conditions in the bottom-near water. Net anoxic conditions within the OMZ might be advantageous methane production (batch incubations) and sulfate reduc- for methanogenic organisms at the sediment-water interface. tion (35S-sulfate radiotracer incubation) were determined in Our results revealed a high relevance of surface methano- the upper 0–25 cm b.s.f. of multiple cores from all stations, genesis on the shelf, where the ratio between surface to deep while deep hydrogenotrophic methanogenesis (> 30 cm b.s.f., (below sulfate penetration) methanogenic activity ranged be- 14C-bicarbonate radiotracer incubation) was determined in tween 0.13 and 105. In addition, methane concentration pro- two gravity cores at selected sites (78 and 407 m). Further- files indicated a partial release of surface methane into the more, stimulation (methanol addition) and inhibition (molyb- water column as well as consumption of methane by anaer- date addition) experiments were carried out to investigate the obic methane oxidation (AOM) in the surface sediment. The relationship between sulfate reduction and methanogenesis. present study suggests that surface methanogenesis might Highest rates of methanogenesis and sulfate reduction play a greater role in benthic methane budgeting than previ- in the surface sediments, integrated over 0–25 cm b.s.f., ously thought, especially for fueling AOM above the sulfate– were observed on the shelf (70–253 m, 0.06–0.1 and methane transition zone. 0.5-4.7 mmol m−2 d−1, respectively), while lowest rates were discovered at the deepest site (1024 m, 0.03 and 0.2 mmol m−2 d−1, respectively). The addition of methanol resulted in significantly higher surface methanogenesis ac- 1 Introduction tivity, suggesting that the process was mostly based on non- competitive substrates – i.e., substrates not used by sulfate Microbial methanogenesis represents the terminal step of or- reducers. In the deeper sediment horizons, where competi- ganic matter degradation in marine sediments (Jørgensen, tion was probably relieved due to the decrease of sulfate, the 2006). The process is entirely restricted to a small group usage of competitive substrates was confirmed by the detec- of prokaryotes within the domain of the Archaea (Thauer, 1998). Methanogens produce methane from a narrow spec- Published by Copernicus Publications on behalf of the European Geosciences Union. 284 J. Maltby et al.: Microbial methanogenesis in the sulfate-reducing zone of surface sediments trum of substrates, primarily carbon dioxide (CO2) and hy- availability of non-competitive substrates (Zinder, 1993; Van drogen (H2) (hydrogenotrophic pathway), as well as acetate Der Maarel and Hansen, 1997). Similarly, methanogenesis (acetoclastic pathway) (Zinder, 1993). In addition, methanol activity was observed within the sulfate-reducing zone of or methylated compounds such as methylamine can be uti- organic-rich sediments from the seasonally hypoxic Limfjor- lized (methylotrophic pathway) (Oremland and Polcin, 1982; den sound, northern Denmark (Jørgensen and Parkes, 2010; Buckley et al., 2008; Zinder, 1993; King et al., 1983). Sub- Jørgensen, 1977). strates for methanogenesis are produced during depolymer- The environmental relevance of surface methanogenesis is ization and fermentation of organic macromolecules (e.g., hitherto unknown. Its closeness to the sediment–water inter- sugars, vitamins, amino acids) to smaller monomeric prod- face makes it a potential source for methane emissions into ucts (Jørgensen, 2006; Schink and Zeikus, 1982; Neill et al., the water column, unless the methane is microbially con- 1978; Donnelly and Dagley, 1980). sumed before escaping the sediment (Knittel and Boetius, Acetoclastic and hydrogenotrophic methanogenesis are 2009). Methane escapes the sediment either by diffusion predominantly found in deeper sediment zones below sul- or, when methane saturation is exceeded, in the form of fate penetration, owing to the more effective utilization of gas bubbles (Whiticar, 1978; Wever and Fiedler, 1995; Judd H2 and acetate by sulfate reducers due to their higher sub- et al., 1997; Dimitrov, 2002). The fraction of methane re- strate affinity (Oremland and Polcin, 1982; Jørgensen, 2006). leased to the water column that reaches the atmosphere Methanogens can avoid competition with sulfate reducers mainly depends on water depth, as methane is also consumed by the utilization of non-competitive substrates, such as within the water column through aerobic microbial oxida- methanol or methylamines (Oremland and Polcin, 1982; tion (Reeburgh, 2007; Valentine et al., 2001). Thus, shallow King et al., 1983). Facilitated by the usage of such non- coastal areas have higher methane emission potentials than competitive substrates, sulfate reduction and methanogene- the open ocean (Bange et al., 1994) and a greater poten- sis were found to co-occur in sulfate-containing salt marsh tial to contribute to methane-dependent atmospheric warm- sediments (Oremland et al., 1982; Buckley et al., 2008; Se- ing (IPCC, 2014). nior et al., 1982). Concurrent activity of sulfate reduction In the present study we focused on the upwelling region and methanogenesis in the marine environment has mostly off the Peruvian coast, which is another example of an en- been postulated for organic-rich sediments (Mitterer, 2010; vironment where both factors that potentially favor surface Jørgensen and Parkes, 2010; Treude et al., 2009, 2005a; methanogenesis convene – i.e., a high export of organic car- Hines and Buck, 1982; Crill and Martens, 1986); however, bon and low dissolved oxygen concentrations in the bottom details on the magnitude and environmental controls of sur- water. This upwelling region represents one of the most pro- face methanogenesis are still poorly understood (Holmer and ductive systems in the world oceans, creating one of the most Kristensen, 1994; Ferdelman et al., 1997). intense oxygen minimum zones (OMZs, Kamykowski and In a study from Eckernförde Bay, southwestern Baltic Sea, Zentara, 1990; Pennington et al., 2006). Oxygen concentra- considerable in vitro methanogenic activity was observed in tions in waters impinging on the seafloor are below 20 µM or samples taken from 5 to 40 cm sediment depth (Treude et al., even reach anoxia. Research on surface sediment methano- 2005a). Although in vitro activity was measured in sulfate- genesis in upwelling regions is scarce and its potential role free setups, methanogenic activity coincided with zones of in the carbon cycling of the Peruvian OMZ is completely un- in situ sulfate reduction. The authors concluded a coexis- known. In a study from the central Chilean upwelling area tence of the two types of organisms, which could be en- (87 m water depth, 0.5–6 cm sediment depth), low methane abled through either the usage of non-competitive substrates, production rates were detected despite high sulfate reduction dormancy of methanogens until phases of sulfate depletion, activity, when the non-competitive substrate trimethylamine and/or temporal or spatial heterogeneity in the sediments. was offered (Ferdelman et al., 1997). The authors concluded Eckernförde Bay sediments feature a high input of organic that the prevailing methanogens were competing with sul- matter due to a shallow water depth (∼ 30 m) and pronounced fate reducers for H2 and with acetogens for methylamines, phytoplankton blooms in spring, summer and fall (Smetacek, explaining the overall low methanogenesis activity observed 1985). Furthermore, seasonal hypoxia (O2 < 90 µM) or even (Ferdelman et al., 1997). anoxia (O2 D0 µM) occur in the deep layers of the water col- Even though the Chilean and Peruvian OMZs are con- umn caused by stratification and degradation of organic mat- nected, commonly known as OMZ in the eastern