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Microbial Methane Production in Oxygenated Water Column of an Oligotrophic Lake

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Microbial Methane Production in Oxygenated Water Column of an Oligotrophic Lake Microbial methane production in oxygenated water column of an oligotrophic lake Hans-Peter Grossarta,b,1, Katharina Frindtea, Claudia Dziallasa, Werner Eckertc, and Kam W. Tangd aDepartment of Limnology of Stratified Lakes, Leibniz-Institute of Freshwater Ecology and Inland Fisheries, D-16775 Stechlin, Germany; bInstitute for Biochemistry and Biology, University of Potsdam, D-14469 Potsdam, Germany; cIsrael Oceanographic and Limnological Research, The Yigal Allon Kinneret Limnological Laboratory, Migdal 14650, Israel; and dVirginia Institute of Marine Science, College of William & Mary, Gloucester Point, VA 23062 Edited by Merritt R. Turetsky, University of Guelph, Guelph, Canada, and accepted by the Editorial Board October 20, 2011 (received for review July 2, 2011) The prevailing paradigm in aquatic science is that microbial Here, we test if microbial methane production occurs in the well- methanogenesis happens primarily in anoxic environments. Here, oxygenated water column of a temperate oligotrophic lake (Lake we used multiple complementary approaches to show that micro- Stechlin, Germany). To obtain conclusive evidence, we established bial methane production could and did occur in the well-oxy- several criteria: (i)verification of methane production even in genated water column of an oligotrophic lake (Lake Stechlin, unamended lake water, (ii)confirmation that DO remains at high Germany). Oversaturation of methane was repeatedly recorded in levels when methane production occurs, and (iii) demonstration of the well-oxygenated upper 10 m of the water column, and the uncoupling between methane production and consumption causing methane maxima coincided with oxygen oversaturation at 6 m. accumulation of methane in well-oxygenated water. Laboratory incubations of unamended epilimnetic lake water and inoculations of photoautotrophs with a lake-enrichment culture Results both led to methane production even in the presence of oxygen, In Situ Methane Profiles and Microbial Composition. Methane and the production was not affected by the addition of inorganic oversaturation was observed within the upper 10 m on July 21 and phosphate or methylated compounds. Methane production was 22, 2010, when the lake was calm and strongly stratified (Fig. 1A). also detected by in-lake incubations of lake water, and the highest A methane maxima of 1.35–1.44 μM coincided with the thermo- – · −1 – production rate was 1.8 2.4 nM h at 6 m, which could explain 33 cline and DO oversaturation at 6 m (Fig. 1 B and C). DO over- SCIENCES 44% of the observed ambient methane accumulation in the same saturation was also present 1 mo earlier (Fig. 1C), coinciding with ENVIRONMENTAL month. Temporal and spatial uncoupling between methanogenesis the chlorophyll (Chl) a peak (Fig. 1D). However, the Chl a max- and methanotrophy was supported by field and laboratory meas- imum was below 10 m on July 22, and the observed DO peak was urements, which also helped explain the oversaturation of meth- likely the result of a past phytoplankton bloom. Microbial abun- ane in the upper water column. Potentially methanogenic Archaea dance was higher in the upper 12 m than below the thermocline, were detected in situ in the oxygenated, methane-rich epilimnion, and of this abundance, 11–40% were particle-associated microbes and their attachment to photoautotrophs might allow for anaero- (Fig. 1E). The dominant autotrophs were the cyanobacterium bic growth and direct transfer of substrates for methane produc- Aphanizomenon flos-aquae and diatoms (Asterionella formosa and tion. Specific PCR on mRNA of the methyl coenzyme M reductase A Fragillaria crotonensis) in the upper 9 m. Free-living methanogenic gene revealed active methanogenesis. Microbial methane produc- Archaea belonging to uncultured Methanomicrobiales were tion in oxygenated water represents a hitherto overlooked source present at 6 m (Fig. S1), and particle-associated methanogenic of methane and can be important for carbon cycling in the aquatic Archaea were found at 6 (closely related to uncultured Meth- environments and water to air methane flux. anomicrobiales and Methanosaeta) and 9 m (closely related to Methanosaeta and the Candidatus Methanoregula sp.) (Fig. S1); epilimnic methane peak | methanogens however, they were undetectable at 18 m. Methane-oxidizing lthough methane makes up <2 parts per million by volume A(ppmv) of the atmosphere, it accounts for 20% of the total Author contributions: H.-P.G., K.F., W.E., and K.W.T. designed research; H.-P.G., K.F., C.D., radiative forcing among all long-lived greenhouse gases (1). In W.E., and K.W.T. performed research; H.-P.G., K.F., C.D., W.E., and K.W.T. analyzed data; and H.-P.G., K.F., W.E., and K.W.T. wrote the paper. the aquatic environments, methane is also an important sub- The authors declare no conflict of interest. strate for microbial production (2). The prevailing paradigm is This article is a PNAS Direct Submission. M.R.T. is a guest editor invited by the Editorial that microbial methanogenesis occurs primarily in anoxic Board. environments (3, 4). A commonly observed paradox is methane Freely available online through the PNAS open access option. accumulation in well-oxygenated waters (2, 5), which is often Data deposition: The sequences reported in this paper have been deposited in the Gen- assumed to be the result of physical transport from anoxic sed- Bank database (accession nos. JF510050–JF510160). – iment and water (6 8) or in situ production within microanoxic 1To whom correspondence should be addressed. E-mail: [email protected]. – zones (9 11). Two recent studies challenged this paradigm and This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. suggested that microbes in oligotrophic ocean can metabolize 1073/pnas.1110716108/-/DCSupplemental. methylated compounds and release methane even aerobically *We estimated oxygen consumption in the experiments in the work by Karl et al. (12) as (12, 13). These claims are not without caveats, because the follows. According to table 2 in ref. 12, particulate carbon increased by 104 μM within amounts of methylated compounds added [1–10 μM methyl- 48 h. Assuming a bacterial growth efficiency of 0.33 and a respiratory quotient of one phosphonate (12) and 50 μM dimethyl sulfoniopropionate (13)] (14), the estimated O2 consumption because of bacterial biomass production would have been 311 μM, which was more than the ambient O2 concentration (205–215 μM) were far higher than their environmental concentrations, and (ref. 12, table 1). Alternatively, based on table 2 in ref. 12, we calculated a dissolved therefore, the ecological relevance remains obscure. Moreover, organic carbon (DOC) consumption of 217 μM within 48 h. Assuming a 1:1.2 molar ratio of DOC oxygen to O2 consumption by microbes (15), the incubation bottles would have dissolved oxygen (DO) was not monitored during the long in- become anoxic in 38–40 h. In the experiments, glucose was added (100–200 μM) to cubation (5–6 d), and the possibility that the experimental setups stimulate bacterial growth, which would also stimulate oxygen consumption. Assuming had become anoxic before methane production could not be a molar ratio of 1 glucose to 6 O2, the addition of glucose would have led to an O2 dismissed.* Despite the uncertainty, if microbial methane pro- consumption of 600–1,200 μM, which is three to six times the oxygen that was present in the water. Hence, using their data and estimating oxygen consumption in various ways, duction can occur in oxygenated water, it will have profound we came to the same conclusion. It is very likely that their incubation bottles had implications for carbon cycling and climate. become anoxic before substantial methane production was observed. www.pnas.org/cgi/doi/10.1073/pnas.1110716108 PNAS Early Edition | 1of5 Downloaded by guest on September 27, 2021 ABCDE Fig. 1. Depth profiles for Lake Stechlin. (A) Mean methane concentrations during day and night (July 21 and 22, 2010, respectively). Error bars during the day are SDs of two to three measurements of the same bottles. Arrow indicates methane concentration in the air. (B) Average temperature on July 21 and 22. (C) Dissolved oxygen (DO) on June 22 and July 22. (D) Chlorophyll (Chl) a concentrations on June 22 and July 22. (E) Free-living and attached microorganism abundances on July 22. bacteria (MOB) were not detectable in the epilimnion, whereas at Methane Production in In-Lake Incubation Experiments. Methane 18 m, a single species of MOB type I (99% similarity to Methyl- production was observed in the first in-lake incubation experi- obacter tundripaludum) was detected. MOB type II were not ment (June 13) (Fig. 2B). The gross methane production rate detectable. varied significantly among water samples suspended at different Repeated measurements in September of 2010 showed tem- depths but not between the light and dark treatments. The highest − poral regression of the methane peak at 6 m, decreasing to only average production rates were at 1.2–1.8 nM·h 1 at 6 m. Methane 0.10 μM by September 12. The reverse temporal development was production was observed again in the second experiment (June − observed in 2011, when the methane peak at 6 m increased from 15) at an even higher average rate of 2.4 nM·h 1 at 6 m (Fig. 2B) 0.18 μM in May to 1.25 μM in June (Fig. S2). As in the previous when in situ methane concentrations had further increased. year, the methane maxima in 2011 coincided with the thermocline and DO oversaturation. We detected the active methyl coenzyme Uncoupled Methane Oxidation in Laboratory Experiments. When M reductase A (mcrA) gene for methanogenesis based on mRNA unamended Lake Stechlin surface water samples were incubated over a longer time, methane concentrations in all three replicates at 6 m in May and June of 2011.
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