the Creative Commons Attribution 4.0 License.
the Creative Commons Attribution 4.0 License.
| 27 Sep 2024
Impact of deoxygenation and hydrological changes on the Black Sea nitrogen cycle during the Last Deglaciation and Holocene
Abstract. The marine nitrogen (N) cycle profoundly impacts global ocean productivity. Amid rising deoxygenation in marine environments due to anthropogenic pressures, understanding the impact of this on the marine N-cycle is vital. The Black Sea’s evolution from an oxygenated lacustrine basin to an anoxic marine environment over the last deglaciation and Holocene offers insight into these dynamics. Here, we generated records of the organic biomarkers heterocyte glycolipids, crenarchaeol, and bacteriohopanetetrol, associated with various water-column microbial N-cycle processes, which indicate a profound change in Black Sea N-cycle dynamics at ~7.2 ka when waters became severely deoxygenated. This transition substantially reduced Thaumarchaeota-driven nitrification and enhanced loss of bioavailable nitrogen through anammox. In contrast, other climatic changes over the last deglaciation and Holocene, such as freshwater input, water-level variations and temperature changes, did not impact these processes. Cyanobacterial nitrogen fixation in surface waters proved more responsive to changes in salinity and associated water column stratification. Our results indicate that future deoxygenation in marine environments may enhance bioavailable nitrogen loss by anammox and reduce nitrification by Thaumarchaeota, while enhanced stratification may increase cyanobacterial nitrogen fixation in the surface waters.
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RC1: 'Comment on cp-2024-59', Anonymous Referee #1, 10 Nov 2024
Overall analysis:
The manuscript by Cutmore et al., offers a thorough and well-rounded analysis of nitrogen cycle dynamics in the Black Sea, covering the period from deglaciation through the Holocene. The use of diverse biomarker proxies and geochemical data provides a solid foundation for the study’s conclusions. The work is valuable not only for understanding past biogeochemical processes but also for its implications on how similar changes could unfold in modern marine environments facing deoxygenation and stratification. The integration of isotopic, lipid biomarker, and microbial evidence is particularly strong, and the study effectively links these proxies to long-term environmental changes.
What I particularly found the strength points of the manuscript include:
Comprehensive approach: The use of multiple lines of evidence (e.g., isotopes, biomarkers, and microbial data) results in a robust dataset, allowing for a detailed reconstruction of changes in the N-cycle across key transitions.
Long-Term perspective: By covering a wide temporal range, the study provides valuable insights into the resilience and shifts in the N-cycle across significant climatic events, including the shift to an anoxic marine basin at 7.2 ka.
Relevance to modern changes: The findings are timely and relevant, as they offer a useful analogy for understanding how current and future shifts in marine stratification and deoxygenation might affect nitrogen cycling.
Strong microbial ecology component: The discussion linking microbial processes (e.g., anammox and Thaumarchaeota activity) with geochemical changes helps bridge paleoclimate research and microbial ecology, making the study multidisciplinary and compelling.
Despite the strong evidence for a stable subsurface N-cycle throughout the Holocene and deglaciation periods, the manuscript does not delve deeply enough into why this stability persisted, despite significant hydrological and climatic changes. The authors convincingly show that the subsurface N-cycle was resilient, but the mechanisms behind this resilience are not explored in detail. For example, it would be useful to discuss the potential roles of microbial community structure, nutrient buffering, or physical mixing processes that might explain this stability? in this regard I would like if the authors could address the following questions:
1. The observed stability of the subsurface N-cycle is a key finding, but there is little discussion on what processes could have maintained this stability. The authors could consider elaborating on potential factors, such as community dynamics or nutrient availability, that might have contributed?
2. The use of hexose glycosides (HG) as indicators of cyanobacterial activity is somewhat speculative, especially given the shifts in salinity and environmental conditions throughout the study period. A more critical evaluation of this proxy’s reliability would strengthen the interpretation. I suggest providing a more critical assessment of the assumption underlying biomarkers proxies, especially HGs.
3. The temporal resolution during critical transitions, particularly around 7.2 ka, may not be high enough to capture rapid or short-term variations in N-cycle dynamics. Acknowledging this limitation and its potentiaal impact on the findings would be helpful
4. The reliance on modern analogues for interpreting past microbial and biogeochemical processes introduces uncertainties, especially given that past environmental conditions co uld differ significantly from present-day scenarios. This should be addressed more explicitly. For instance, the authors could expand the discussion a little bit to include a more nuanced view, highlighting the uncertainties of extrapolating modern findings to past conditions.
Detailed comments:
Line 30: remove "our", in "the global oceans" sounds more scientific
Line 35: The term Anammox was used in the abstract without introduction, and this is the first time it is introduced, I would add the complete term in abstract as well.
Line 120-121: I would avoid using "with" twice, perhaps you can change with heated electrospray ionization to "using heated..."
Line 216: Clarify if "C32 triol pentose that are specific to cyanobacteria symbiotic with diatoms" mean a marine source or the earlier mentioned freshwater/brackish environments?
Figure comments:
I have one major comment regarding the use of figures in the manuscript. As a general rule, figures that are referenced more than twice should be included in the main text. Figures S2, S3, S4, and S5 are mentioned more than five times each, indicating that they will be of significant interest to the audience. Including them in the supplements makes it more difficult for readers to refer to them easily. I recommend moving at least Figure S2 into the main text. Supplements should be only for figures/material that are "supplementary" to understanding of the manuscript.
Citation: https://doi.org/10.5194/cp-2024-59-RC1 -
AC1: 'Reply on RC1', Anna Cutmore, 17 Jan 2025
We are very grateful for the detailed, thoughtful and helpful comments. Below, please find our point-by-point response and how we intend to address your comments.
- The observed stability of the subsurface N-cycle is a key finding, but there is little discussion on what processes could have maintained this stability. The authors could consider elaborating on potential factors, such as community dynamics or nutrient availability, that might have contributed.
Thank you for this feedback. We will ensure that there is a more thorough discussion on the potential factors that maintained the stability of the subsurface N-cycle in our revised manuscript. It is likely that the significant changes to the basin (i.e. freshwater input, water-level variations and temperature changes) primarily affected the surface waters and due to the stratification of the basin, and did not have such a significant effect on the sub-surface waters, which led to relatively stable habitat for these microbes, leading to stability in the subsurface N-cycle.
- The use of hexose glycosides (HG) as indicators of cyanobacterial activity is somewhat speculative, especially given the shifts in salinity and environmental conditions throughout the study period. A more critical evaluation of this proxy’s reliability would strengthen the interpretation. I suggest providing a more critical assessment of the assumption underlying biomarkers proxies, especially HGs.
Thank you for this suggestion. In the manuscript, we will provide a more critical evaluation of the use and assumptions of using HGs as an indicator of cyanobacterial activity.
- The temporal resolution during critical transitions, particularly around 7.2 ka, may not be high enough to capture rapid or short-term variations in N-cycle dynamics. Acknowledging this limitation and its potential impact on the findings would be helpful
Thank you for this comment. While this record shows centennial scale changes, we acknowledge that there may be decadal scale N-cycle changes that are outside of the scope of this project but are of scientific interest for future work. We will ensure the limitations of this, and its implications on the findings, are acknowledged in the manuscript.
- The reliance on modern analogues for interpreting past microbial and biogeochemical processes introduces uncertainties, especially given that past environmental conditions could differ significantly from present-day scenarios. This should be addressed more explicitly. For instance, the authors could expand the discussion a little bit to include a more nuanced view, highlighting the uncertainties of extrapolating modern findings to past conditions.
This is indeed a significant limitation of all proxies of environmental change, and we will ensure that this important point is stated in the discussion.
Thank you for the helpful detailed comments, we have addressed them all as follows:
Line 30: we will change “our” to “the”
Line 35: we will add the complete anammox term to the abstract
Line 120-121: we will change to "using heated..."
Line 216: we will clarify that these diatoms have a marine source
Figure comments:
We agree that it is hard to follow having so many figures that are important to the story in the supplement. We will move the most mentioned S1 and S2 to the main text.
Citation: https://doi.org/10.5194/cp-2024-59-AC1
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AC1: 'Reply on RC1', Anna Cutmore, 17 Jan 2025
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RC2: 'Comment on cp-2024-59', Anonymous Referee #2, 26 Dec 2024
Cutmore et al. present a detailed study using new organic biomarker data (e.g., heterocyte glycolipids, crenarchaeol, bacteriohopanetetrol) and d15N records from the Black Sea to investigate nitrogen cycle changes over the past 20,000 years. Similar to previous studies of Black Sea history, this study documents the transition of the Black Sea from an oxygenated lacustrine basin to an anoxic marine environment. Significant shifts in the nitrogen cycle are identified between 9.7 and 7.2 ka as the basin reconnected to the global ocean, leading to stratification and anoxic conditions. These changes include increased nitrogen fixation and anammox activity, as well as reduced nitrification by Thaumarchaeota.
The biomarker data are compelling and align well with the broader understanding of Black Sea evolution since the early Holocene. The interpretations are generally logical and provide valuable insights into aquatic nitrogen cycle dynamics. However, there are several key areas where the manuscript could be improved to strengthen its clarity.
Major Comments
- Implications for future ocean deoxygenation: While the study provides valuable insights into the aquatic nitrogen cycle, it is highly unlikely that future ocean deoxygenation might lead to euxinic conditions similar to the Black Sea. There is no evidence of sulfidic waters in the modern global ocean, even in the most oxygen-depleted zones, such as the eastern tropical Pacific, which still contain significant nitrate concentrations. Furthermore, no model projections suggest that oxygen-deficient zones will evolve toward euxinia under global warming scenarios. The authors should conduct a thorough literature review and clarify this point to avoid potential confusion.
- Stratification-induced nitrogen fixation: The authors conclude that stratification led to increased nitrogen fixation since 7.2 ka and suggest that future ocean stratification could similarly enhance nitrogen fixation. This extrapolation from the Black Sea to the global ocean is problematic. Stratification alone does not directly enhance nitrogen fixation. Rather, nitrogen fixation is more directly influenced by nitrogen limitation relative to phosphorus. In the modern Black Sea, intense nitrogen limitation, driven by anammox-induced nitrogen loss in the subsurface, is the key driver of surface nitrogen fixation. Enhanced stratification slows the upward supply of ammonium and promotes fixed nitrogen loss through anammox, indirectly increasing surface nitrogen limitation. A more detailed discussion connecting these paleo-data to modern Black Sea and global ocean observations is essential to contextualize these findings.
- Riverine nitrogen input: Previous studies have suggested that riverine nitrogen input is a major source of fixed nitrogen in the modern Black Sea. The authors should discuss how riverine nitrogen input might influence their paleo-records and whether it impacts their interpretations of nitrogen cycle dynamics.
- Comparison with existing d15N records: The study presents a new d15N record, but comparisons with existing records (e.g., Fulton et al., 2012) are limited. A direct comparison of these d15N records, ideally plotted together, would highlight potential consistencies or discrepancies and strengthen the study. In addition, as the authors point out, bulk sedimentary d15N is well-known to reflect mixed signals; and its limitations should be discussed thoroughly.
- Diagenesis and preservation bias: Bulk sedimentary d15N and biomarkers such as BHT-x and crenarchaeol are prone to diagenesis and preservation biases, which could complicate interpretations of microbial population dynamics. The authors should discuss how such biases may affect their results and the reliability of their conclusions.
Minor Comments
- Line 23-24: As mentioned above, specify the mechanisms by which salinity and stratification affect cyanobacterial nitrogen fixation.
- Adding a figure showing modern water column chemical data (e.g., oxygen, nitrate, and ammonium profiles) would provide essential context for readers unfamiliar with the Black Sea.
- Table 1: Table 1 is not directly referenced in the discussion and could be moved to the supplementary materials. In contrast, I found that supplementary figures such as S1, S2, S5, and S6 are highly informative and should be included in the main manuscript for accessibility.
- Figure 1: Add descriptions of depth contours.
Citation: https://doi.org/10.5194/cp-2024-59-RC2 -
AC2: 'Reply on RC2', Anna Cutmore, 17 Jan 2025
Thank you for the comprehensive and helpful comments. Please find our point-by-point response and how we intend to address your comments, below:
Major Comments
- Implications for future ocean deoxygenation: While the study provides valuable insights into the aquatic nitrogen cycle, it is highly unlikely that future ocean deoxygenation might lead to euxinic conditions similar to the Black Sea. There is no evidence of sulfidic waters in the modern global ocean, even in the most oxygen-depleted zones, such as the eastern tropical Pacific, which still contain significant nitrate concentrations. Furthermore, no model projections suggest that oxygen-deficient zones will evolve toward euxinia under global warming scenarios. The authors should conduct a thorough literature review and clarify this point to avoid potential confusion.
Thank you for this valuable comment. We will go through the manuscript to ensure that we are not suggesting that future global deoxygenation will always result in euxinia. We will ensure that we clarify that we are discussing N-cycle processes that are not specific to euxinia and that occur widely across various non-euxinic basins (i.e. nitrification by Thaumarchaeota, N-fixation by cyanobacteria and anammox by planctomycete bacteria), and are therefore not the result of euxinia, but influenced by changes in oxygenation of the Black Sea basin.
- Stratification-induced nitrogen fixation: The authors conclude that stratification led to increased nitrogen fixation since 7.2 ka and suggest that future ocean stratification could similarly enhance nitrogen fixation. This extrapolation from the Black Sea to the global ocean is problematic. Stratification alone does not directly enhance nitrogen fixation. Rather, nitrogen fixation is more directly influenced by nitrogen limitation relative to phosphorus. In the modern Black Sea, intense nitrogen limitation, driven by anammox-induced nitrogen loss in the subsurface, is the key driver of surface nitrogen fixation. Enhanced stratification slows the upward supply of ammonium and promotes fixed nitrogen loss through anammox, indirectly increasing surface nitrogen limitation. A more detailed discussion connecting these paleo-data to modern Black Sea and global ocean observations is essential to contextualize these findings.
Thank you for this comment. We will go through the manuscript and ensure that we are not extrapolating to the global ocean. We will also ensure there is more discussion relating to the N limitation relative to P in the modern ocean and assessing the link to our palaeo-records.
- Riverine nitrogen input: Previous studies have suggested that riverine nitrogen input is a major source of fixed nitrogen in the modern Black Sea. The authors should discuss how riverine nitrogen input might influence their paleo-records and whether it impacts their interpretations of nitrogen cycle dynamics.
We will include references to riverine nitrogen input in the modern Black Sea but feel that it is unlikely to have influenced the Black Sea N-cycle over the Last Deglaciation and Holocene at our location to a large degree due to its remoteness from the coast. We will address this in our manuscript.
- Comparison with existing d15N records: The study presents a new d15N record, but comparisons with existing records (e.g., Fulton et al., 2012) are limited. A direct comparison of these d15N records, ideally plotted together, would highlight potential consistencies or discrepancies and strengthen the study. In addition, as the authors point out, bulk sedimentary d15N is well-known to reflect mixed signals; and its limitations should be discussed thoroughly.
Thank you for this suggestion. We will ensure there is a more thorough comparison of our d15N record to that of Fulton et al., 2012, and there will be a more thorough discussion of the limitations of bulk d15N records.
- Diagenesis and preservation bias: Bulk sedimentary d15N and biomarkers such as BHT-x and crenarchaeol are prone to diagenesis and preservation biases, which could complicate interpretations of microbial population dynamics. The authors should discuss how such biases may affect their results and the reliability of their conclusions.
We agree that the possibility of diagenesis and preservation bias of the biomarkers in the Black Sea record needs to be addressed in the manuscript and will ensure that this point is included in the manuscript. We think that it likely has not played a major role in our records since large parts of the water column remained low in oxygenation and consequently organic carbon contents remained relatively high.
Minor Comments
Thank you for these suggestions, we have address them all as follows:
- Line 23-24: We will specify the mechanisms by which salinity and stratification affect cyanobacterial nitrogen fixation to this section.
- We agree that this is helpful information, add to the “Regional Setting” section information about modern water column chemical data (oxygen, nitrate, and ammonium profiles) in the Black Sea.
- Thank you for this suggestion, we will move Table 1 to the supplementary material and the most referenced figures, S1 and S2, to the main manuscript.
- Figure 1: We will add descriptions of depth contours
Citation: https://doi.org/10.5194/cp-2024-59-AC2
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