Biogeochemical and Physical Controls on Methane Fluxes from Two Ferruginous Meromictic Lakes
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Received: 27 March 2019 | Revised: 20 August 2019 | Accepted: 31 August 2019 DOI: 10.1111/gbi.12365 ORIGINAL ARTICLE Biogeochemical and physical controls on methane fluxes from two ferruginous meromictic lakes Nicholas Lambrecht1 | Sergei Katsev2,3 | Chad Wittkop4 | Steven J. Hall5 | Cody S. Sheik3,6 | Aude Picard7 | Mojtaba Fakhraee3 | Elizabeth D. Swanner1 1Department of Geological and Atmospheric Sciences, Iowa State University, Ames, IA, Abstract USA Meromictic lakes with anoxic bottom waters often have active methane cycles 2 Department of Physics, University of whereby methane is generally produced biogenically under anoxic conditions and Minnesota Duluth, Duluth, MN, USA 3Large Lakes Observatory, University of oxidized in oxic surface waters prior to reaching the atmosphere. Lakes that contain Minnesota Duluth, Duluth, MN, USA dissolved ferrous iron in their deep waters (i.e., ferruginous) are rare, but valuable, 4 Department of Chemistry and as geochemical analogues of the conditions that dominated the Earth's oceans dur‐ Geology, Minnesota State University, Mankato, MN, USA ing the Precambrian when interactions between the iron and methane cycles could 5Department of Ecology, Evolution, and have shaped the greenhouse regulation of the planet's climate. Here, we explored Organismal Biology, Iowa State University, controls on the methane fluxes from Brownie Lake and Canyon Lake, two ferrugi‐ Ames, IA, USA 6Department of Biology, University of nous meromictic lakes that contain similar concentrations (max. >1 mM) of dissolved Minnesota Duluth, Duluth, MN, USA methane in their bottom waters. The order Methanobacteriales was the dominant 7 School of Life Sciences, University of methanogen detected in both lakes. At Brownie Lake, methanogen abundance, an Nevada Las Vegas, Las Vegas, NV, USA increase in methane concentration with respect to depths closer to the sediment, Correspondence and isotopic data suggest methanogenesis is an active process in the anoxic water Nicholas Lambrecht, Department of Geological and Atmospheric Sciences, Iowa column. At Canyon Lake, methanogenesis occurred primarily in the sediment. The State University, 2337 Osborn Drive, Ames, most abundant aerobic methane‐oxidizing bacteria present in both water columns IA 50011, USA. Email: [email protected] were associated with the Gammaproteobacteria, with little evidence of anaerobic methane oxidizing organisms being present or active. Direct measurements at the Funding information NSF, Grant/Award Number: EAR ‐ 1660691, surface revealed a methane flux from Brownie Lake that was two orders of magni‐ EAR ‐ 1660761 and EAR ‐ 1660873; tude greater than the flux from Canyon Lake. Comparison of measured versus calcu‐ Huron Mountain Wildlife Foundation; Canada Foundation for Innovation; Natural lated turbulent diffusive fluxes indicates that most of the methane flux at Brownie Sciences and Engineering Research Council Lake was non‐diffusive. Although the turbulent diffusive methane flux at Canyon of Canada; University of Saskatchewan; Government of Saskatchewan; Western Lake was attenuated by methane oxidizing bacteria, dissolved methane was detected Economic Diversification Canada; National in the epilimnion, suggestive of lateral transport of methane from littoral sediments. Research Council Canada; Canadian Institutes of Health Research These results highlight the importance of direct measurements in estimating the total methane flux from water columns, and that non‐diffusive transport of methane may be important to consider from other ferruginous systems. KEYWORDS ferruginous, lakes, meromictic, methane flux The complete dataset for all values in all figures can be found at the following DOI: https ://doi.org/10.6073/pasta/ 58e69 64173 07565 55069 631eb c687a61 Geobiology. 2019;00:1–16. wileyonlinelibrary.com/journal/gbi © 2019 John Wiley & Sons Ltd | 1 2 | LAMBRECHT et al. 1 | INTRODUCTION pervasive ferruginous conditions below the mixed layer throughout much of Earth's history (Poulton & Canfield, 2011). Understanding Ferruginous (Fe‐rich and anoxic) lakes that are meromictic (i.e., per‐ factors that control CH4 cycling from ferruginous systems can manently stratified with respect to salinity) have been noted for their help discern how carbon was cycled under the geochemical con‐ active CH4 cycles, which includes the biological production of CH4 in ditions of early Earth. The focus on CH4 extends out of the water the anoxic sediment, and diffusion of CH4 into the overlying water column as it is one of the main gases thought to have regulated column where oxidation occurs (although, see Pasche et al. (2011) early Earth climate in the Archean. Paleoatmospheric modeling for alternative methanogenic pathways in volcanic lakes such as the suggests that CH4 was an important greenhouse gas, in addition to reduction of geogenic CO2). Slow vertical mixing and anoxic bottom CO2, that warmed Earth during the lower solar luminosity experi‐ ‐ 2‐ waters that are depleted of electron acceptors (e.g., NO3 and SO4 ) enced in the Archean Eon (see Olson, Schwieterman, Reinhard, & lead to the accumulation of CH4 in the water column. Lyons, 2018 and references therein). As soon as methanogenesis Methane production rates under ferruginous conditions de‐ evolved ~3.5 Ga (Ueno, Yamada, Yoshida, Maruyama, & Isozaki, pend on the importance of methanogenesis relative to other or‐ 2006; Wolfe & Fournier, 2018), CH4 could begin to accumulate 2‐ ganic carbon mineralization pathways, such as SO4 and Fe(III) in the reduced Archean atmosphere. In the absence of O2,H C 4 reduction. Thermodynamic considerations suggest the presence of is estimated to have reached a maximum of ~50× pre‐industrial Fe(III)‐(hydr)oxides should promote Fe(III) reduction and preclude atmospheric levels (ca. 700 ppb; Etheridge, Steele, Francey, & methanogenesis (Reeburgh, 2007). This is due to the relative energy Langenfelds, 1998) assuming pCO2 near upper paleosol limits microbes yield from Fe(III) reduction coupled to organic matter ox‐ (Olson et al., 2018). After the “Great Oxidation Event” (ca. 2.4 Ga), idation, which can be 10s of times more than the energy yielded by pCH4 n i the atmosphere is estimated to have decreased to ~25 methanogenesis (Lovley & Chapelle, 1995). However, in ferruginous ppmv by the mid‐Proterozoic due to microbial oxidation mitigating settings at circumneutral pH, Fe(II) is several orders of magnitude CH4 fluxes (Fakhraee, Hancisse, Canfield, Crowe, & Katsev, 2019). more soluble than Fe(III) (Thamdrup, 2011) and can sorb to the sur‐ Specifically, O2‐induced continental sulfide weathering introduced 2‐ 2‐ faces of Fe(III)‐(hydr)oxides that may form at an oxic–anoxic bound‐ SO4 to the oceans where SO4 ‐based AOM diminished the flux ary. This interaction renders the Fe(III)‐(hydr)oxides less accessible of CH4 drastically (Canfield, 2005; Catling, Claire, & Zahnle, 2007). 2‐ to Fe(III)‐reducing microbes (Roden & Urrutia, 1999, 2002). Despite the introduction of SO4 , ferruginous oceanic conditions In general, archaea mediate the production of CH4 through persisted throughout most of Earth's history until the oxygenation methanogenesis, and CH4 production in lakes usually occurs in the of the deep oceans around 0.58 Ga (Canfield, Poulton, & Narbonne, sediments (Rudd & Hamilton, 1978). The oxidation of CH4 n i lakes 2007; Poulton & Canfield, 2011). has largely been noted to occur at the oxic–anoxic boundary by aer‐ What ways can CH4 e b emitted from ferruginous meromictic obic methane‐oxidizing bacteria (MOB; Hanson and Hanson, 1996), lakes? Substantial CH4 oemission t the atmosphere via non‐diffusive with fewer observations of anaerobic oxidation of methane (AOM) transport has been shown to occur out of water columns <100 m by anaerobic methanotrophic archaea (ANME) (e.g., Eller, Känel, & deep (McGinnis, Greinert, Artemov, Beaubien, & Wüest, 2006). Of Krüger, 2005; Schubert et al., 2011). To date, the microbial cycling of the ferruginous meromictic lakes studied where the water columns CH4 has been investigated in only a handful of ferruginous meromic‐ are less than this threshold (Lake La Cruz and Lake Svetloe), the CH4 tic lakes, including Lake La Cruz, Lake Matano, Lake Svetloe, Woods flux has not been directly measured. Further, does the CH4 flux differ Lake, and Lake Pavin (Biderre‐Petit et al., 2011; Crowe et al., 2011; among ferruginous meromictic lakes where a disparity in maximum Dupuis, Sprague, Docherty, & Koretsky, 2019; Oswald, Jegge, et al., depth exists? We set out to explore CH4 biogeochemical dynamics in 2016a; Savvichev et al., 2017). two ferruginous lakes to answer these questions. Brownie Lake and Despite the permanently high CH4 reservoir in ferruginous Canyon Lake are two meromictic lakes in the Midwest, U.S.A., that meromictic lakes, CH4 ofluxes t the atmosphere are estimated to be have anoxic and Fe‐rich bottom waters (>1 mM dissolved Fe below low based on vertical reaction‐transport modeling of water column the chemocline; Lambrecht, Wittkop, Katsev, Fakhraee, & Swanner, CH4 concentrations, which is biased toward turbulent diffusion as a 2018). Our goal was to evaluate the role of diffusive and non‐diffu‐ transport mechanism. In one instance at Lake La Cruz, the aerobic sive CH4 ofluxes t the atmosphere and quantify these CH4 nfluxes i 2‐ MOB are suggested to mitigate all CH4 emissions (Oswald, Milucka, et our two ferruginous lakes with different SO4 concentrations. More 2‐ al., 2016b). In other lakes (e.g., Kabuno Bay of Lake Kivu, Lake Pavin, precisely,