Substrate potential of last interglacial to Holocene permafrost organic matter for future microbial greenhouse gas production

Stapel, Janina G.; Schwamborn, Georg; Schirrmeister, Lutz; Horsfield, Brian; Mangelsdorf, Kai

doi:https://doi.org/10.5194/bg-15-1969-2018

Articles | Volume 15, issue 7

https://doi.org/10.5194/bg-15-1969-2018

© Author(s) 2018. This work is distributed under
the Creative Commons Attribution 3.0 License.

https://doi.org/10.5194/bg-15-1969-2018

© Author(s) 2018. This work is distributed under
the Creative Commons Attribution 3.0 License.

Articles | Volume 15, issue 7

Research article

|

04 Apr 2018

Research article |

| 04 Apr 2018

Substrate potential of last interglacial to Holocene permafrost organic matter for future microbial greenhouse gas production

Janina G. Stapel, Georg Schwamborn, Lutz Schirrmeister, Brian Horsfield, and Kai Mangelsdorf

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Final revised paper (published on 04 Apr 2018)
Supplement to the final revised paper
Preprint (discussion started on 17 Mar 2017)

Interactive discussion

Status: closed

AC: Author comment | RC: Referee comment | SC: Short comment | EC: Editor comment

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- Supplement

RC1: 'Review of Stapel et al', Anonymous Referee #1, 13 Apr 2017
- AC1: 'Responses to the reviewer#1', Janina Stapel, 07 Jul 2017
RC2: 'Referee comment', Anonymous Referee #2, 08 May 2017
- AC2: 'Responses to the reviewer#2', Janina Stapel, 07 Jul 2017
RC3: 'Review of Stapel et al', R. Sparkes, 11 Jun 2017
- AC3: 'Responses to the reviewer#3; R.Sparkes', Janina Stapel, 07 Jul 2017

Peer-review completion

AR: Author's response | RR: Referee report | ED: Editor decision

ED: Reconsider after major revisions (10 Jul 2017) by Jack Middelburg

AR by Janina Stapel on behalf of the Authors (26 Jul 2017) Author's response Manuscript

ED: Referee Nomination & Report Request started (08 Aug 2017) by Jack Middelburg

RR by Anonymous Referee #2 (12 Aug 2017)

Suggestions for revision or reasons for rejection

General comments
I find the manuscript improved, but also that some of my concerns have been only partly addressed (previous comments 1, 2, 4, 8):
(1) I agree with the authors that chemical composition of organic matter can influence its degradability. However, we know that chemical composition is not the only factor involved. Since the data on chemical composition of organic matter presented here are used to make conclusions about its degradability, I think a comment on other parameters that can have an impact is necessary, and that the data need to be discussed more carefully. Apart from temperature, I am for instance thinking of oxic versus anoxic conditions and association with soil minerals.
(2) I still find the motivation for looking at past and present microbial biomarkers poorly justified. For instance, on page 12, lines 7-8, the authors write: “In order to investigate whether the freeze-locked OM already stimulated a microbial community during deposition in the past, biomarkers for past microbial communities were examined.” Why would anybody assume otherwise? Microorganisms exist in almost every environment. There is no reason to assume that there were no microbial communities in the Pleistocene.
(4) Please add a list with the specific compounds considered for total PLFAs. There is a lot of variation between different studies.
(8) While my technical comments have been addressed, there are plenty of new grammatical errors and unclear sentences (see below). Please check your language and consult a professional service if necessary.

Further general comments:
(10) I find the discussion of soil moisture conditions during deposition very speculative (e.g., page 13, lines 13-28).

Technical corrections
Page 2, line 7: “resulted in”.
Page 2, line 9: Delete “again”.
Page 2, line 12: “enhanced”. I’m also not sure what you mean with “microbial production”. Activity? Growth?
Page 2, lines 13-14: I suggest a separate sentence for the global change feedback.
Page 2, line 15: Delete “in”.
Page 2, line 18: “at today’s coasts and islands”. You could also delete the insert.
Page 2, line 19: Split the sentence. E.g., “These deposits provide a unique paleo-environmental archive … “
Page 2, line 21: What do you mean with “here”?
Page 2, lines 30-31: This sentence is incomprehensible. I suggest: “We selected Bol’shoy Lyakhovsky Island in the Laptev Sea (NE Siberia) as our study area, since it provides an excellent opportunity to investigate permafrost OM deposited from the last interglacial to the Holocene.”
Page 2, lines 33-34: I suggest: “These Eemian depostis form a paleo-equivalent to the Holocene and are otherwise rather difficult to assess.”
Page 3, line 2: “Oyogos Yar”
Page 4, lines 26-28: Please add a reference.
Page 5, line 28: I think the reference should be in brackets.
Page 5, line 29: With C1-C5 gases, do you mean alkanes?
Page 6, line 4: What other anions? This is the only time this is mentioned. If other compounds were quantified originally but are not presented in this paper, I would not mention them.
Page 6, line 23: Change “were” to “was”.
Page 6, line 25: What do you mean with “optical correlations”?
Page 6, line 29: Add “communities” after “bacterial”.
Page 6, line 30: The bracket after “archaeal communities” is incomprehensible.
Page 7, line 22: Add a “the” to the “TOC curve”.
Page 8, line 7: How is R2=0.8, p=0.021 not a significant correlation?
Page 9, line 16: Remove “of”.
Page 10, line 6: Remove “again”.
Page 10, line 9: Remove “rich” in both cases.
Page 10, lines 8-14: See my general comments on organic matter chemistry. I do not question that chemical composition is important, but I think a more balanced view is necessary. Further, I don’t find it justified to claim that pyrolysis is established here as a new tool. It has been frequently used before and the ending of the sentence (“… as introduced in Stapel et al….”) is in fact a contradiction to that claim. The sentence in lines 10-12 is also not clear.
Page 10, lines 20-21: This interpretation implies that there is strong algal growth now in the active layer. Is there any evidence for this from previous studies that use different approaches?
Page 10, line 30: Nitrogen is not respired, please re-phrase.
Page 10, lines 28-31: A common mechanism that can lead to low TOC/TN values is soils is the accumulation of inorganic N (binding of ammonium to clay minerals).
Page 11, line 6: Dryer.
Page 11, line 17: Change “into” to “in”.
Page 11, line 27: Change “setting” to “settings”.
Page 11, line 28: “Reveals”.
Page 12, line 3: What do you mean with “higher rates of decomposed OM”?
Page 12, line 14: “contain bacteria and archaea”.
Page 12, lines 18-19: Do you mean labile carbon in the permafrost?
Page 13, line 1: “varies between”.
Page 13, line 3: “markers”.
Page 13, lines 6-7: There is some mixup in the text.
Page 13, line 9: I would change “greenhouse gas production” to “methane production”.
Page 13, lines 9-11: What do you mean? I thought the whole paragraph is about correlations between TOC and past microbial markers.
Page 13, lines 13-14: Please add a “might” or “is expected to” or similar.
Page 13, line 30: Please clarify which periods the thermokarst lakes refer to.
Page 14, line 3: Change to “… did not significantly affect the concentration …”
Page 14, lines 6-7: Please re-phrase. This sentence is incomprehensible.
Page 14, line 26: I don’t find anything on the input of old and new carbon and a stimulation of microbial activity in the cited paper.
Page 14, line 27: “result in”.
Page 14, line 30 to page 15, line 6: Do you mean that when the active layer is deepened and reaches the now frozen MIS 3, 4, and 1 deposits, we expect a microbial biomass similar to the current active layer, and microbial consumption of the contained acetate? Can you write this more clearly?
Page 15, line 8: Article missing (“… that the free-acetate pool …”)
Page 15, line 17: I would replace “caused by the onset of the early Holocene” by “at the onset of the early Holocene”. I suppose this is what you mean.
Page 16, lines 7-8: Please specific what you mean with “concerning” here.
Page 3, lines 15-16: I don’t understand, please rephrase.

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RR by Anonymous Referee #1 (24 Aug 2017)

Suggestions for revision or reasons for rejection

Based on the comments of 3 reviewers, Stapel et al have revised their manuscript on substrate potential of permafrost OM for greenhouse gas production. The current version the manuscript has improved compared to the first version, but still needs further improvement in order to be acceptable for publication in Biogeosciences. Next to the interpretation (see detailed comments below), also the grammar will need a more thorough check. The long sentences, grammatical mistakes, and needless repetitions distract from bringing the main message across.

Based on reviewers comments (in random order):
- OM quality
There is no clear definition of OM ‘quality ‘in the introduction, and to me it is not clear what is exactly meant by ‘quality’, and what makes the quality of OM of good or bad. To me it would make more sense if the terms OM composition and/or OM properties are being used. Or even OM biodegradability. Since OM ‘quality’ is what the paper is about, this needs to be clarified.
A better definition may also prevent strange constructions like on P3L6-9: To access (better: obtain?) information on quality in terms of biodegradability of freeze locked OM, we examined characteristic OM parameters (amount and quality) and LMWOAs. In other words: you assess quality in order to examine quality….

- Since biomarker concentrations and TOC follow the same trends, both reviewer 1 and 3 suggest to normalize biomarker data on TOC. Doing this would help make the case that downcore trends in biomarker concentrations are real, and not related to changes in TOC. In their rebuttal, the authors indicate that biomarker trends remain after normalizing. To prevent future readers asking the same question, I strongly suggest to present TOC normalized data in the next version.

- source of OM (terrestrial vs lacustrine)
As already pointed out by reviewers 1 and 3 there are still contradictions in the description of the source of OM in the permafrost deposits. The origin is claimed to be terrestrial, but site descriptions clearly mention that the depositional environment was lacustrine. Also, all aliphatic-rich sediments are attributed an algal source. This needs to be discussed or stated more carefully.

- past vs present biomass (reviewer 1 comments 8 and 11)
I get that you choose to use PLFAs as a marker for living biomass, but I still don’t see how that automatically makes GDGTs markers for past biomass. If you want to use GDGTs as such, you will have to provide a reference, or present this as a finding of this study rather than introducing them this way. Be careful with the ether-ester bond interpretation for the qualification of fossil/living-derived lipids, as this concerns headgroups, and not bonds within membrane lipids.
The extraction technique used here only extracts core lipid GDGTs. The vast majority of the GDGT pool in soils (also modern ones) is present as core lipid, so their presence as such does not tell you anything about the vitality of the microbial community, in past nor present. Instead you would have to look at IPL-GDGTs, i.e. with a phospho- or glyco-headgroup attached, and then I do agree that the phospho-GDGTs (attached with an ester bond) would indeed be a better marker for living organisms than glyco-GDGTs (attached with an ether bond).

- Comment 10 of reviewer 1: Space wise I can see why you choose to plot isoGDGT-0 and archaeol in the same panel. However, since they do not necessarily share the same source, please plot them as separate lines, so it is clear when they follow the same trend and when they do not.

- Introduction:
The transition to the paragraph with the study area (P2L30) is still very sudden. From the previous section it is not clear what the open question actually is that will be addressed in this study. This only starts to make sense after reading the actual aim in the very last paragraph on P3L26. I suggest to move this paragraph up, prior to the site introduction.
The permafrost feedback that is the whole driver of this study can also be better introduced, as it is now only mentioned on the side (P2L13).

- Results:
The results are presented as values, rather than what they really are (e.g. concentrations). For example, P7L8: TOC values instead of TOC concentration. Check this in the whole section.

- Statistics: I am happy to see that the authors have included statistical support for their statements.

Textual (a selection, the text needs editing):
P1L16:…acetate are used.
P1L16: replace highest by largest (pool)
P1L17: …pools in permafrost are present in the layers that cover MIS3 and MIS4.
P1L18: …deposits from MIS5e contain only a small pool of substrate.
P2L8: replace formerly preserved OM by accumulated OM
P2L14: replace Previous by former
P2L15: remove comma after in
P2L31: ‘The last interglacial deposits have been interpreted as Eemian’ -> of course they are, otherwise they would not be from the last interglacial.
P4L24: replace which are distinct between by which occur between
P4L28: how can a site drain and then freeze over?
P5L16: indicate how samples were decalcified (with HCl?)
P6L4: indicate that free acetate was measured in the pore water
P8L7: curves do not correlate but have R2 of 0.8, p=0.02? Seems like a nice correlation to me though…
P8L16: How can you have an average concentration in a range?

P11L30: if you use significant provide p-value
P12L7: how can OM stimulate a microbial community? I think you need to rephrase.
P12L12: archaeol without a headgroup is not an IPL! See earlier comment on IPL vs CLs and present vs past biomarkers

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ED: Reconsider after major revisions (24 Aug 2017) by Jack Middelburg

AR by Janina Stapel on behalf of the Authors (23 Dec 2017) Author's response Manuscript

ED: Referee Nomination & Report Request started (04 Jan 2018) by Jack Middelburg

RR by Anonymous Referee #2 (15 Jan 2018)

RR by Anonymous Referee #1 (22 Jan 2018)

Suggestions for revision or reasons for rejection

The structure of the introduction has improved and is much clearer now. Also many of the grammatical errors have been corrected, although a few new ones have emerged in the revised parts of the manuscript. I still have a few comments that should be addressed prior to publication in BGS:

P1, L12: …,which form….
P1, L17: …pyrolysis experiments on the…
P2, L49: These deposits provide….
P3, L73: replace ‘applied’ by ‘performed’. Or even better, adjust the whole sentence to: In addition, microbial biomarkers such as….are analyzed to examine…
P4L107: add the IR-OSL age.
P4:125: This line confused me earlier. I don’t think soils freeze over. Lakes do, but soils/sediments just freeze. Delete ‘over’ (but check with a native speaker if you can).
L201-205: Can you add how PLFAs were identified? In particular the position of branches/unsaturations/presence of rings (rather than unsaturation).
L205: ‘The sum of all brGDGTs (…) varies between xx and xx, while concentrations of the….’
L234: …but reach their maximum at a different depth.
L298-305: This paragraph should go to the introduction.
L312: add the TOC concentration between brackets. I have no idea what a ‘typical concentration’ is for a Yedoma deposit…
L316: Since you do not present any results that directly support the thermokarst environment during the Holocene and Eemian, add a reference after the statement that Holocene and Eemian sediments are deposited in a thermokarst environment. This seems quite important given your sub-conclusion in the last paragraph of this section.
L316: The BIT index is not properly introduced, nor are BIT index values presented in the results section. At least mention brGDGTs as soil end-member and crenarchaeol (currently not introduced at all) as marine end-member, being produced by marine algae. Consequently, soils are characterized by high BIT index values, and marine sediments by low BIT index values.
As for your specific setting: BIT index values in lake sediments are not well understood (see e.g. Blaga et al 2009 J. Paleolimn. or Blaga et al 2011 GCA), and can easily reach values op to 1 as well, as the BIT index can be influenced by Thaumarchaea and (unknown) aquatic brGDGT-producers (e.g. Tierney et al., 2010 GCA, Weber et al., 2015 GCA). Hence, the BIT index is not a very reliable tool to differentiate between soils and thermokarst/lake material. The only statement I would be comfortable making is that BIT index values in your permafrost material are high, and thus have a terrestrial origin (as opposed to marine).
L320ff: Try to avoid using samples, but instead mention the type of sediment. In this case active layer material. This makes it easier to follow what deposit is being discussed.
L338: replace dryer by drier.
L349: Peterse et al 2014??
L365: replace ‘as to’ by ‘on’.
L380: decreased compared to what? Other layers? Or over time?
I don’t understand the next sentence. Life marker signals represent living community…
L410: ‘warmer conditions’ or ‘higher temperatures’.
L413: Stapel et al 2017 is not listed in the references.
L417: …suggest lower soil-moisture content in the active…
L418: An explanation for the lower soil-moisture content is that all cores…
L424-425: this is exactly the reason why I asked earlier to normalize biomarker data to TOC, as this makes a fairer comparison than comparing g biomarker/g sediment. It would make sense to use the TOC-normalized brGDGT concentrations here too.
Also, these last few lines seem a bit out of place here, and should better fit with the discussion on the sources of OC in the different permafrost layers.
L470: As a consequence, or consequently.
L482: Thus, in contrast to simply using the…
L490: these

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ED: Publish subject to minor revisions (review by editor) (24 Jan 2018) by Jack Middelburg

AR by Janina Stapel on behalf of the Authors (02 Feb 2018) Author's response Manuscript

ED: Publish subject to technical corrections (06 Feb 2018) by Jack Middelburg

Dear Dr. Stapel and Dr. Mangelsdorf:

I have read your paper in detail and I am sorry to tell you that I am a little disappointed about the presentation quality since this is version 4. The science is fine but the writing needs improvement. I nevertheless have decided to accept your paper pending further technical corrections. Congratulations, but please make these corrections and try to improve your writing further. After that and editorial office corrections your paper will likely make a nice contribution to the literature.

Thank you for considering Biogeosciences as your outlet,

Jack Middelburg, Associate Editor

Technical corrections:
• All through please check your use of past vs. present tense. For instance, in the abstract many sentences should have been written in past tense.
• The use of marine isotope stages and Holocene, Eemian is somewhat confusing (some section use MIS, others Eemian, different authors?) and please introduce MIS before first use, both in abstract and in main text.
• Line 62: are suggested to (by who??).
• Line 70: On the one and on the other hand always go together
• Line 73: were analysed/analysed
• Line 141: deposits were deposited: reformulate
• Line 145: grinding, samples
• Line 162: rpm have no meaning, use g-force
• Line 163: were measured in pore-water samples
• All through, use construction like from x to y and vary between x and y. Do not use a mixture. (there are many of these misuses)
• Line 208: vary between 849.1 and 27.2…
• Line 238: all past markers were high (results so in past tense and use high rather than strongly increased, because increased from what).
• Line 243: reformulate: are indicated
• Line 344: .. 3) for the Eemian deposits (…) showed a more….
• Line 367: on how the
• Line 488: OM with high HI..
• Concentration are reported in mg/L for acetate. Is this acetate or mg C/L. I guess the former as most organic geochemist report, but many biogeochemist report on C basis. Inform the reader.

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AR by Janina Stapel on behalf of the Authors (14 Feb 2018) Author's response Manuscript

Post-review adjustments

AA: Author's adjustment | EA: Editor approval

AA by Kai Mangelsdorff on behalf of the Authors (29 Mar 2018) Author's adjustment Manuscript

EA: Adjustments approved (29 Mar 2018) by Jack Middelburg

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Short summary

Climate warming in the Arctic results in thawing of permafrost deposits. This promotes the accessibility of freeze-locked old organic matter (OM) accumulated during the past. Characterizing OM of different depositional ages, we were able to show that OM from last glacial Yedoma deposits possess the highest potential to provide organic substrates such as acetate for microbial greenhouse gas production and therefore to accelerate the carbon–climate feedback cycle during ongoing global warming.