28 Jan 2021
28 Jan 2021
Methane oxidation in the waters of a humics-rich boreal lake stimulated by photosynthesis, nitrite, Fe(III) and humics
- 1Department of Surface Waters – Research and Management, EAWAG, Swiss Federal Institute of Aquatic Science and Technology, Kastanienbaum, Switzerland
- 2Institute of Biogeochemistry and Pollutant Dynamics, ETH Zurich, Swiss Federal Institute of Technology, Zurich, Switzerland
- 3School of Architecture, Civil and Environmental Engineering, EPFL, Swiss Federal Institute of Technology, Lausanne, Switzerland
- 4Department of Environmental Sciences, Aquatic and Stable Isotope Biogeochemistry, University of Basel, Basel, Switzerland
- These authors contributed equally to this work.
- 1Department of Surface Waters – Research and Management, EAWAG, Swiss Federal Institute of Aquatic Science and Technology, Kastanienbaum, Switzerland
- 2Institute of Biogeochemistry and Pollutant Dynamics, ETH Zurich, Swiss Federal Institute of Technology, Zurich, Switzerland
- 3School of Architecture, Civil and Environmental Engineering, EPFL, Swiss Federal Institute of Technology, Lausanne, Switzerland
- 4Department of Environmental Sciences, Aquatic and Stable Isotope Biogeochemistry, University of Basel, Basel, Switzerland
- These authors contributed equally to this work.
Abstract. Small boreal lakes are known to contribute significantly to global methane emissions. Lake Lovojärvi is a eutrophic lake in Southern Finland with bottom water methane concentrations up to 2 mM. However, the surface water concentration, and thus the diffusive emission potential, was low (< 0.5 μM). We studied the biogeochemical processes involved in methane removal by chemical profiling and through incubation experiments. δ13C-CH4 profiling of the water column revealed methane-oxidation hotspots just below the oxycline and within the anoxic water column. In incubation experiments involving the addition of light and/or oxygen, methane oxidation rates in the anoxic hypolimnion were enhanced 3-fold, suggesting a major role for photosynthetically fueled aerobic methane oxidation. A distinct peak in methane concentration was observed at the chlorophyll a maximum, caused by either in-situ methane production or other methane inputs such as lateral transport from the littoral zone. In the dark anoxic water column at 7 m depth, nitrite seemed to be the key electron acceptor involved in methane oxidation, yet additions of Fe(III), anthraquinone-2,6-disulfonate and humic substances also stimulated anoxic methane oxidation. Surprisingly, nitrite seemed to inhibit methane oxidation at all other depths. Overall, this study shows that photosynthetically fueled methane oxidation can be a key process in methane removal in the water column of humic, turbid lakes, thereby limiting diffusive methane emissions from boreal lakes. Yet, it also highlights the potential importance of a whole suite of alternative electron acceptors, including humics, in these freshwater environments in the absence of light and oxygen.
- Preprint
(874 KB) -
Supplement
(397 KB) - BibTeX
- EndNote
Sigrid van Grinsven et al.
Status: open (until 11 Mar 2021)
-
CC1: 'Comment on bg-2021-3', Antti Rissanen, 03 Feb 2021
reply
It was really interesting to read a study on methane oxidation conducted in the same study lake as our recent study (Rissanen et al. FEMS Microb Ecol, Volume 97, Issue 2, February 2021, fiaa252). While our study was focused on the genetic potential of methanotrophs, this study provides very valuable novel information on the various factors affecting the activity of methanotrophs in boreal lakes. Here are some minor suggestions, which I think could further improve the manuscript:
Line 49-52. It is perhaps worth to mention here study by Zheng et al. 2020 on extracellular electron transfer from methane to Fe-mineral by Methylomonas in hypoxic conditions.
https://pubs.acs.org/doi/abs/10.1021/acs.estlett.0c00436
Line 69-70. Either “can play” or “are likely to play”
Line 73-74 and in especially discussion. Maybe it would be relevant to mention and discuss your results also in the light of our previous study from 2018, which was conducted in the nearby humic boreal lakes, where we also studied lake water methane oxidation with amendments of various EAs (incl. NO3, metals, organic EAs) and in different light conditions, and also studied the community structure and genetic potential of methanotroph communities (Rissanen et al. 2018):
https://www.int-res.com/abstracts/ame/v81/n3/p257-276/
Furthermore, study by Kallistova et al. (2018) might be also relevant to mention and discuss. They also studied methane oxidation and MOB communities in water column of a boreal lake.
https://www.int-res.com/abstracts/ame/v82/n1/p1-18/
Line 87-. Study site. It is maybe worth to mention the historical anthropogenic effects, the soaking of flax and hemp, which potentially have contributed to the (chemical) stratification in the lake. In the Finnish publication (Tolonen et al. 1976), it is mentioned in Finnish that “Hampun ja myöhemmin myös pellavan liotus nopeuttivat läheisen Lovojärven pilaantumista jo rautakaudella (Huttunen & Tolonen 1975).” = Soaking of hemp and later also soaking of flax accelerated the pollution of nearby Lake Lovojärvi already during Iron Age”.
Tolonen K, Tolonen M, Honkasalo L et al. Esihistoriallisen ja historiallisen maankäytön vaikutuksesta Lammin Lampellonjärven kehitykseen. Luonnon Tutkija. 1976;80:1–15 (in Finnish with English abstract):
https://www.researchgate.net/publication/311665698_Esihistoriallisen_ja_historiallisen_maankayton_vaikutus_Lammin_Lampellonjarven_kehitykseen_The_influence_of_of_prehistoric_and_historic_land_use_on_Lake_Lampellonjarvi_South_Finland
Unfortunately, I could not find the original reference of Huttunen & Tolonen 1975.
Line 118. were fixed
Line 382- What about archaea-driven methanogenesis in anoxic micro-niches?
Also more generally, there are recent studies suggesting that also methanogenic archaea can oxidize methane anaerobically, e.g. via extracellular electron transfer to solid EAs (iron minerals, organic EAs, anode in bioelectrochemical systems). Maybe worth to mention and discuss. See, e.g.
https://www.sciencedirect.com/science/article/abs/pii/S1385894720328199
https://pubmed.ncbi.nlm.nih.gov/28965392/
Line 468-470. Our study in the same study lake (which has been cited but not in this context) detected genetic potential for nitrate/nitrite/NO – reduction as well as for extracellular electron transfer (to metal minerals and organic EAs) in metagenome assembled genomes of Methylocococcales (incl. Methylobacter sp. and the Crenothrix-type MOB), which supports the results of this study on enhancement of methane oxidation by these various EAs. See:
https://academic.oup.com/femsec/article/97/2/fiaa252/6034011
Line 473-481. Microbial interactions. Maybe worth to include and discuss also the results by Cabrol et al. 2020. They studied anaerobic methane oxidation (AOM) and MOB communities in water columns of northern lakes and found correlation between Methylococcales and OTUs within Methylotenera, Geothrix and Geobacter genera which indicated that AOM might occur in an interaction between MOB, denitrifiers and iron-cycling partners.
https://www.sciencedirect.com/science/article/pii/S0048969720331053
Figure 1. Is there a slight increase in O2 towards the deepest depths (from appr. 15 m to the deepest depth)? If there is, what is causing it?
References:
Kortelainen et al. 2000. Numbers as subscripts for CH4, CO2 and N2O
Mutyaba 2012. Maybe it could be mentioned that it is Master of Science thesis. And perhaps provide a link to it. https://jyx.jyu.fi/handle/123456789/40735
Rissanen et al. DOI-link is missing.
-
RC1: 'Comment on bg-2021-3', Anonymous Referee #1, 22 Feb 2021
reply
This interesting study investigates the biogeochemical methane cycle in a relatively shallow, eutrophic boreal lake using a wide range of chemical, microbiological and molecular techniques. The authors show that the lake Lovojärvi has a very active methane cycle mostly driven by upwards diffusing methane from the sediment (produced by methanogenesis) but also provide evidence for an additional source of methane within the water column near the Chla maxium. Methane seems to be efficiently consumed by the microbial community, in particular at the oxic-anoxic interface as well as in the anoxic hypolimnion. Using 13C-methane incubations, the authors show that methane oxidation in the anoxic hypolimnion seems to be coupled to in situ production of oxygen at shallower depths, while some of the tested electron acceptors appear to stimulate methane oxidation in the dark anoxic hypolimnion. Furthermore, FISH and 16S rRNA amplicon analyses indicate that alpha- and gammaproteobacterial methanotrophs appear to be the dominant methanotrophs.
Overall I find this study very interesting. Considering that boreal lakes are quite poorly characterized in respect to methane cycling, I believe that this study is a valuable addition to the current literature. The manuscript nicely highlights that light-driven methane oxidation as well as AOM coupled to other electron acceptors can be important processes in the anoxic hypolimnion of shallow boreal lakes. The evidence for photosynthesis-fueled methanotrophy appears robust und the authors do a good job discussing some of the observed anomalies (e.g. +O2 vs. light, 3 m vs. 4 m). However, I’m more skeptical about proposed stimulation of MOR by some of the amended substrates, in particular AQDS, and I feel that the authors should be more careful not to overstate the results of their incubation experiments (see point #1). Other than that, I have only minor suggestions. The manuscript is generally well written and understandable, and the Methods are rather brief but for the most part adequately described. The introduction could be more focused on methane cycling in boreal lakes in general (see point #2) and it would be helpful if the authors could provide some context around why Lovojärvi was studied (see point #3).
Specific points:
#1 Stimulation of MOR in incubations
For some incubations, there is a clear increase in MOR (e.g. light) and the data looks robust to me. However, for other incubations the stimulation is much less pronounced (e.g. Fe, humic acid) or even so small that the difference is in my opinion within the margin of error (for AQDS). Without independent biological replicate incubations, which I don’t think the authors did (please correct me if I’m wrong), I am not entirely convinced that the presented data for AQDS (and possibly Fe and humic acid) conclusively show a stimulation of MOR. As it is an interesting and important conclusion, I encourage the authors to provide some additional data (e.g. statistical tests) to support their claims.
#2 Introduction could be more focused on boreal lakes
In its current form, the introduction is very general. While I agree that boreal lakes are not excessively studied, I believe that more can be said in the introduction than that “studies […] are relatively scant”. I encourage the authors to expand their introduction with more information about biological methane oxidation in boreal lakes (e.g. what is known about humic substances and why are they important, availability of other TEA, are they often Fe- and Mn-rich?).
#3 Boreal lakes and Lovojärvi
Lovojärvi strikes me as a quite unique lake (presence of halocline, extreme CH4 concentration above the sediment, meromixis). Is this a typical boreal lake with typical physico-chemical features? Since the authors use their findings to make general conclusions regarding the biological methane filter and the emission potential in boreal lakes (e.g. lines 14-18), it would be important to include some discussion/description on how representative Lovojärvi is for boreal lakes in general.
Minor points:
Line 64: “aerobic MOB” sounds counterintuitive in this context. Please rephrase.
Line 73: There is definitely more literature available on methane oxidation in boreal lakes (e.g. Rissanen et al. 2017, https://doi.org/10.1093/femsec/fix078)
Line 164: How much water was typically filtered?
Line 174: How many cells were counted?
Line 191: Include some information regarding sequencing depth (either here or as a table)
Line 233: The NOx profiles are quite stunning. I assume that the nitrate and nitrite peak close to the base of the oxycline are due to microbial ammonia oxidation. But what could be the source of nitrite in the bottom water?
lines 292: The meaning of ‘other Methylococcaceae’ is unclear to me. Please specify.
lines 292-296: I’m confused. Methylocystaceae abundance seems low but this sentence suggests to me that they might be high since you detected unknown Rhizobiales bacteria? Please clarify.
lines 283-301: It’s not clear to me according to what logic the abundances of different methanotrophs, methylotrophs and some seemingly random taxa (Acidoferax, Planctomycetaceae, Rhizobiales) are listed one after the other. Please restructure. Also, some of these groups are never discussed and it’s not clear why they are specifically mentioned here.
Line 290: Were you able to observe any filamentous gamma-MOB using FISH?
line 311: “natural conditions” suggests that different light intensities were used for incubations from 3m and 7, please clarify.
Line 319: Given the uncertainties in Table S3, AQDS 5m MOR increase does not look significant.
line 348: What is meant by a concentration of +/- 0.5 uM ?
line 392-401: It would be interesting if the authors could slightly expand on methanogenesis by phototrophs by including some brief speculation what cyanobacterial groups could be responsible for this (using the amplicon data).
Lines 486-488: The contribution of methanotrophs is indeed important, however, I suppose the halocline also plays an important role?
Fig 1: This is quite a busy figure that could use some improvement. I suggest that change the scale of the x-axis for oxygen to highlight the O2 dynamics the lower concentration range (as shown in Fig. S1). In panel A, it looks as if oxygen concentration increases slightly in the hypolimnion, please comment (also in Fig. 2). In panel C, value for MOR – NO2 at 7 m is clearly <1.5 while table S3 shows a value of 1.54. Please explain error bars in legend.
Overall I suggest that the authors revise it to improve clarity. For example: i) not all x-axis same length (panesl C and D) or ii) error bars sometimes not visible.
Fig 2: In my opinion, the y-axis could be limited to 10 m in order to focus on the upper water column.
Fig 3. Only cosmetic, but there is an offset between lines and symbols.
-
RC2: 'Comment on bg-2021-3', Anonymous Referee #2, 25 Feb 2021
reply
The comment was uploaded in the form of a supplement: https://bg.copernicus.org/preprints/bg-2021-3/bg-2021-3-RC2-supplement.pdf
Sigrid van Grinsven et al.
Supplement
Sigrid van Grinsven et al.
Viewed
HTML | XML | Total | Supplement | BibTeX | EndNote | |
---|---|---|---|---|---|---|
384 | 71 | 11 | 466 | 27 | 1 | 2 |
- HTML: 384
- PDF: 71
- XML: 11
- Total: 466
- Supplement: 27
- BibTeX: 1
- EndNote: 2
Viewed (geographical distribution)
Country | # | Views | % |
---|
Total: | 0 |
HTML: | 0 |
PDF: | 0 |
XML: | 0 |
- 1