Reviews and syntheses: Contribution of sulfate to methane oxidation in upland soils: a mini-review

Su, Rui; Li, Kexin; Wang, Nannan; Yuan, Fenghui; Zhao, Ying; Zuo, Yunjiang; Sun, Ying; He, Liyuan; Xu, Xiaofeng; Zhang, Lihua

doi:https://doi.org/10.5194/egusphere-2024-3347

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https://doi.org/10.5194/egusphere-2024-3347

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29 Nov 2024

| 29 Nov 2024

Reviews and syntheses: Contribution of sulfate to methane oxidation in upland soils: a mini-review

Rui Su, Kexin Li, Nannan Wang, Fenghui Yuan, Ying Zhao, Yunjiang Zuo, Ying Sun, Liyuan He, Xiaofeng Xu, and Lihua Zhang

Abstract. Methane (CH₄) is a potent greenhouse gas, its global warming potential is 25 times higher than carbon dioxide (CO₂), and various environmental factors influence CH₄ oxidation in soil. Sulfate (SO₄^2-) ion is the main component of atmospheric deposition and has been increasing in recent years, it promotes CH₄ production and anaerobic CH₄ oxidation, however, the impact of SO₄^2- on CH₄ oxidation remains inconclusive. Due to the limited research on the effects of SO₄^2- on CH₄ oxidation, we synthesize current research on the effects of SO₄^2- on CH₄ oxidation, examining both its direct impact and its influence on the dynamics of soil substances, and the potential indirect effects of SO₄^2- on CH₄ oxidation. Through a literature review, we identified that SO₄^2- facilitates CH₄ oxidation within a range of 3–42 %, moreover, it has been found that various physicochemical properties and processes in the soil are influenced by the addition of SO₄^2-, which in turn affects CH₄ oxidation. This review enhances our understanding of the role of SO₄^2- in promoting CH₄ oxidation and lays the foundation for future studies aimed at validating these findings by quantifying CH₄ flux and oxidation rates, as well as elucidating the underlying microbial processes via experimental research. This review deepens the comprehension of atmospheric CH₄ flux and the global CH₄ cycle, particularly in the context of potential global environmental changes.

Received: 28 Oct 2024 – Discussion started: 29 Nov 2024

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Rui Su, Kexin Li, Nannan Wang, Fenghui Yuan, Ying Zhao, Yunjiang Zuo, Ying Sun, Liyuan He, Xiaofeng Xu, and Lihua Zhang

Status: final response (author comments only)

CC1:
'Comment on egusphere-2024-3347', Yongchuan Yang, 02 Jan 2025

Hello author, I have a question to ask you. Why did you think of sorting out the relationship between sulfate ions and methane oxidation？

Citation: https://doi.org/10.5194/egusphere-2024-3347-CC1
- AC1: 'Reply on CC1', lihua zhang, 04 Jan 2025
  
  Thank you for your comment. I would like to clarify our investigation into the relationship between SO₄^2- and CH₄ oxidation. First, previous studies have shown that SO₄^2- promotes the anaerobic oxidation of CH₄, as SO₄^2- serves as an electron acceptor in this process. Second, SO₄^2- inhibits CH₄ production primarily due to its thermodynamic and kinetic preference as an electron acceptor. Third, based on above two key processes in the CH₄ cycle being influenced by SO₄^2-, we hypothesize that SO₄^2- might also affect CH₄ oxidation, a process that has been shown to be promoted by SO₄^2- in some studies. Thus, we aim to clarify the relationship between SO₄^2- and CH₄ oxidation, as well as potential connections, through this review, providing a foundation for future experiments on the impact of SO₄^2- on CH₄ oxidation. Finally, we have conducted indoor incubation experiments that confirm SO₄^2- does indeed influence CH₄ oxidation and promotes it. We are currently writing up the results of these experiments and plan to publish them soon, which will further support the findings presented in this review. These are my answers and I hope they clear up your doubts.
  
  Citation: https://doi.org/10.5194/egusphere-2024-3347-AC1
RC1:
'Comment on egusphere-2024-3347', Anonymous Referee #1, 02 Jan 2025
The authors aimed to review on direct and indirect contributions of sulfate to methane oxidation in upland soils. As far as I’m concerned, influence of sulfate on methane oxidation is an important topic in biogeochemistry, but the current manuscript failed to make a clear and concise presentation. Here I list my major concerns as follows.
1) Methane oxidation or aerobic methane oxidation?
The manuscript is entitled ‘Contribution of sulfate to methane oxidation...’, but throughout the manuscript the authors seemed to talk only about aerobic methane oxidation. Note that both aerobic and anaerobic methane oxidation exist in upland soils. If the authors just want to review on aerobic methane oxidation processes, please change the title into ‘…Contribution of sulfate to aerobic methane oxidation…’. If not, previous studies regarding anaerobic methane oxidation should also be reviewed in the manuscript.
2) Direct effects?
The authors stated that ‘This review provides a comprehensive summary of the direct and potential indirect impacts of SO₄^2- on CH₄oxidation’ (L. 82 - 84), but I cannot see how sulfate directly influences methane oxidation in the manuscript. It seems that the authors tried to figure out the direct effect in the third part of the manuscript (L. 186 – 250), but they only concluded that ‘due to the scarcity of studies investigating the direct effect of SO₄^2- on CH₄ oxidation, no definitive conclusion regarding its impact could be drawn’ (L. 245 - 247).
Before discussing direct impacts of sulfate on methane oxidation, the authors should first answer whether sulfate could directly influence methane oxidation. Unfortunately, the authors didn’t even try to demonstrate existence of direct influence of sulfate on methane oxidation, but they made a conclusion that they provided ‘a comprehensive summary of the direct and potential indirect impacts’. Therefore, I think the conclusion regarding direct impacts should be modified throughout the manuscript.
From my perspective, direct effects of sulfate on methane oxidation is associated with coupling of anaerobic methane oxidation to sulfate reduction. Under anoxic conditions, numerous studies have demonstrated that sulfate could be the electron acceptor for methane oxidation, which can be considered a direct effect of sulfate on methane oxidation. However, the authors didn’t review on aerobic methane oxidation in the current manuscript.
3) Concerns regarding the major conclusion
From table 1, the authors drew the conclusion that ‘the enhancement of SO₄^2-on CH₄ oxidation is prominent in numerous studies’ (L. 74) and that ‘SO₄^2- facilitates CH₄ oxidation within a range of 3-42%’ (L. 75). However, table 1 only contains results from 5 study sites, and no effect of sulfate addition was observed in 2 out of the 5 sites. In the 5 sites, effects of sulfate addition are 0%, 0%, 3%, 25% and 42%, respectively, and no statistical analysis has been conducted to support the statement that sulfate facilitate methane oxidation by 3-42%. Therefore, I think this conclusion is greatly undermined because of insufficient literature and lack of effective statistics. Additionally, title of table 1 is ‘Promotion effect of sulfate on methane oxidation in diverse biome soils’, but I don’t think 5 forests could be called “diverse biome”.
4) Concerns regarding manuscript structure
I also have some concerns regarding structure of the manuscript. First, the authors spent 2 pages introducing the methane oxidation processes and associated microbes (Pages 4 - 5), which are not much associated with the main topic of the manuscript. These contents are not reviewed in the following parts, and I suggest the authors to shorten these contents. Second, Lines 174 – 182 in section 2.3 repeated contents in the introduction (Lines 60 - 68). Similar sentences also emerged in the implication section (Lines 355 - 360). Third, contents in section 3 are disorganized, and I suggest the authors to reorganize these contents (e. g. by adding a topic sentence to the beginning of each paragraph of this section). Forth, presentation of table 1 (L. 75 - 78) should be in the result section (e.g. section 3), instead of the introduction.
Minor points:
Omission of conjunctions. Grammatically, clauses should be joined by conjunctions, but conjunctions in many places are omitted in the manuscript, especially in the abstract. For example, Lines 16, 20, 21 and 26.

There should be no line feed in ‘Norway Scots Pine forest’ in Table 1 (the first column, the forth row).
Citation: https://doi.org/10.5194/egusphere-2024-3347-RC1
- AC2:
  'Reply on RC1', lihua zhang, 08 Jan 2025
  
  I have uploaded our answer to your question as a file, please check it out.
  
  Citation: https://doi.org/10.5194/egusphere-2024-3347-AC2
  - RC2: 'Reply on AC2', Anonymous Referee #1, 13 Jan 2025
    
    Hi Lihua, I'm glad to see your willingness to address my comments. Your responses are overall satisfactory, while I think you should take note of the following two problems.
    First, you may misunderstand my Point 2. Before addressing this point, you should first distinguish gross effect, direct effect and indirect effect. For example, the ‘3-42%’ effect in your manuscript is the gross effect (not direct effect) of sulfate on methane oxidation, and the gross effect can then be partitioned into direct and indirect effects. In your manuscript, you said that ‘This review provides a comprehensive summary of the direct and potential indirect impacts of SO42- on CH4 oxidation’. What I expect from this statement is that you might have categorized the gross effect into different aspects of direct and indirect effects, but you actually didn’t.
    Second, the conclusion of 3-42% promotion is inaccurate without effective statistical tests. Additionally, the effect size in the 5 studies should be 0%, 0%, 3%, 25% and 42%, but why did you ignore the two sites of no effect when drawing the conclusion of 3-42% promotion?
    Additionally, here are two papers containing results regarding influence of sulfate on aerobic methane oxidation, which may be of help:
    1 Roland, F. A. E. et al. Anaerobic methane oxidation and aerobic methane production African great lake (Lake Kivu) in an east. Journal of Great Lakes Research 44, 1183-1193, doi:10.1016/j.jglr.2018.04.003 (2018).
    2 Kumaraswamy, S., Ramakrishnan, B. & Sethunathan, N. Methane production and oxidation in an anoxic rice soil as influenced by inorganic redox species. Journal of Environmental Quality 30, 2195-2201, doi:10.2134/jeq2001.2195 (2001).
    
    Citation: https://doi.org/10.5194/egusphere-2024-3347-RC2
    
    AC3: 'Reply on RC2', lihua zhang, 23 Jan 2025
    
    I understand your point, and it seems that the misunderstanding was caused by our imprecise phrasing. What we actually meant in the article is the direct impact pathway and the indirect impact pathway, rather than direct effects and indirect effects. Our focus is on arid or semi-arid grasslands, where we summarize the impact of SO₄^2- on aerobic CH₄ oxidation rate in these two types of ecosystems. The direct impact pathway refers to the influence of SO₄^2- on the macro-rate of aerobic CH₄ oxidation, without considering any microscopic mechanisms. It simply looks at how much SO₄^2- affects the CH₄ oxidation rate under aerobic conditions. The indirect impact pathway refers to the changes in soil physical and chemical properties, microorganisms, etc., after SO₄^2- enters the soil, and these changes then indirectly affect the CH₄ oxidation processes. We will revise the terms "direct effects" and "indirect effects" in the article to "direct impact pathway" and "indirect impact pathway."
    
    Regarding your second point, we believe that there are too few studies on the influence of SO₄^2- on aerobic CH₄ oxidation. It is not possible to draw a clear conclusion about the impact of SO₄^2- on aerobic CH₄ oxidation based solely on these five references. Therefore, we have only included these five studies as references. However, it was indeed an oversight on our part to omit the two studies showing a 0% impact. We will revise the statement from "SO₄^2-facilitates CH₄ oxidation within a range of 3-42%" (L. 75) to "SO₄^2- facilitates CH₄ oxidation within a range of 0-42%."
    
    These are all of my responses to your questions. I hope this addresses your concerns. And thank you for providing the two references. It has been helpful in clarifying our thoughts.
    
    Citation: https://doi.org/10.5194/egusphere-2024-3347-AC3
RC3:
'Comment on egusphere-2024-3347', Anonymous Referee #2, 25 Jan 2025

The authors aimed to review the recent literature regarding the impact of sulfate on aerobic methane oxidation in soils. Indeed, this is in interesting biogeochemical topic, given that in the past the focus was on the role of SO₄^2- on anaerobic methane oxidation. I am in agreement with the first reviewer that the current manuscript failed to present the state of knowledge in a clear way and although this is a mini-review, it lacks depth. At the current state, for me, the aim of this manuscript is to show how little research has been done on the influence of sulfate on aerobic methane oxidation and not to summarize the research to date into an overall picture (review) and to point out specific starting points for further studies (syntheses). If I have understood correctly, the authors are currently working on another manuscript including experiments to observe the effects of SO₄^2- on aerobic methane oxidation. By shortening the text considerably and formulating it more precisely, it would be ideally suited as an introduction and part of the discussion for such a manuscript.
In the following, I have outlined my major points for each section and provided more detailed feedback in the comments of the attached document.

1) The introduction would benefit from enhanced clarity, with the relocation of sections from section 4 having the potential to significantly improve its quality. However, the text does not provide a compelling rationale for why the impact of SO₄^2- on aerobic methane oxidation could be of interest. Furthermore, some of the references utilized (marked in the PDF) do not correspond to the original works cited in the text, and some references are employed incorrectly.
2) It is imperative to briefly outline the pathway through which methane is oxidized by methanotrophs, highlighting the genera responsible for this process. However, the focus should be on the enzymes that may be influenced by sulfate, either directly or indirectly, through changes in pH. Additionally, it would be intriguing to examine the effects of sulfate on changes in the methanotrophic community or their abundance. If these aspects are not addressed, it would be advisable to combine and significantly shorten these sections. The topic of high and low affinity methanotrophy is not addressed at all, despite the fact that this distinction is very important because high affinity methanotrophs mainly oxidize atmospheric methane, whereas low affinity methanotrophs focus on the methane produced in the soil. If the authors want to argue that sulfate addition increases the atmospheric soil sink, this is of utmost importance, especially as some of the indirect effects may only target one of the two groups. For instance, the inhibition of methanogenesis would primarily affect the oxidation of methane by low-affinity methanotrophs, while the atmospheric sink may remain unaltered.
In addition, the methanotroph types are nowadays only defined by phylogeny and not as mentioned by their metabolic pathways, membranes etc.
Most of section 2.3 can be moved to the introduction and the rest should be discussed in sections 3 or 4.
3) I find the titles of section 3 and 4 misleading, as most of the processes described in section 3 are indirect effects of SO₄^2- on methane oxidation Moreover, a substantial portion of the argumentation appears to suggest that the primary effect of the sulfate is to mitigate the inhibitory effects of the ammonium. However, it is subsequently presented as that sulfate increases methane oxidation rates. This should be clarified.
4) This section provides a description of the various soil properties that may be influenced by SO₄^2-, yet the processes by which these properties are influenced are only described in rudimentary terms and often unstructured. The impact of SO₄^2- is often speculated. Consequently, this section lacks in depth and needs to be reworked. Furthermore, the sections 5 and 6 should be reworked and combined.

Citation: https://doi.org/10.5194/egusphere-2024-3347-RC3
- AC4:
  'Reply on RC3', lihua zhang, 26 Jan 2025
  Thank you for your comments. We understand your point. We had placed too much emphasis on the limited research regarding SO₄^2-'s effect on aerobic methane oxidation, without synthesizing these studies into a cohesive summary. Based on your suggestion, we will revise this section and present the relevant literature as a unified whole.
  
  
  In fact, we treated Section 4 as a separate part, aimed at validating the impact of SO₄^2-on aerobic methane oxidation. It serves as a supplement to the five studies that investigate SO₄^2-’s effect on aerobic methane oxidation. Among these five studies, two found that SO₄^2- does not affect aerobic methane oxidation, while three observed that SO₄^2- promotes methane oxidation, albeit to varying degrees. By reviewing the possible pathways through which SO₄^2- could influence aerobic methane oxidation, we aim to further support the conclusion that SO₄^2- does indeed affect methane oxidation. We will address the cited literature issues you pointed out by revising them according to your comments and our own searches. Regarding how SO₄^2- impacts aerobic methane oxidation, there are no clear experimental validations, nor any studies specifically investigating the effects of SO₄^2- on aerobic methanotrophs, which is why it is not discussed in the current review.
  
  Currently, no studies have specifically addressed the impact of SO₄^2- on the pathways of aerobic methane oxidation or its effects on methanotrophs. It remains unclear which enzymes or which specific steps in the aerobic methane oxidation process are influenced by SO₄^2-, and how SO₄^2- affects methanotrophs. Therefore, this is not reflected in the review. We will add information regarding high-affinity and low-affinity methanotrophs in the revised version of the manuscript.
  
  We believe that SO₄^2- alleviates the inhibitory effect of ammonium on aerobic methane oxidation due to its promoting effect on the process. There are very few articles on the impact of SO₄^2- on aerobic methane oxidation, and no studies addressing the effects of SO₄^2- on the enzymes involved in aerobic methane oxidation or on the methanotrophs. Therefore, we can only extract potential information from existing literature regarding the promotion of aerobic methane oxidation by SO₄^2- and reflect this in our paper. Sections 3 and 4 will be further refined to provide a clearer and more comprehensive explanation.
  
  We have reviewed all articles that discuss the impact of SO₄^2- on soil and have specifically looked for studies that explore how these effects might influence aerobic methane oxidation. Given the lack of research on the indirect pathways by which SO₄^2- affects aerobic methane oxidation, we can only provide an initial description of SO₄^2-’s impact based on the existing literature. Although preliminary, we believe this description is valid because the effects mentioned are already supported by documented research. For parts 5 and 6, we will revise and merge them later.
  
  That's my response. Thank you again for your comments.
  
  Citation: https://doi.org/10.5194/egusphere-2024-3347-AC4

Rui Su, Kexin Li, Nannan Wang, Fenghui Yuan, Ying Zhao, Yunjiang Zuo, Ying Sun, Liyuan He, Xiaofeng Xu, and Lihua Zhang

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Short summary

This research examines the effect of sulfate on methane oxidation in soil, finding that sulfate may facilitate methane oxidation. Considering methane's role as a greenhouse gas and rising sulfate deposition, the study aims to predict changes in methane oxidation due to acid deposition. Future experiments will explore microbial mechanisms, as sulfate reduces methane emissions while enhancing its consumption, providing insights for mitigation strategies.


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