Novel hot spring Thermoproteota support vertical inheritance of ammonia oxidation and carbon fixation in Nitrososphaeria
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Aerobic ammonia oxidation is crucial to the nitrogen cycle and is only known to be performed by a small number of bacterial lineages (Ammonia Oxidizing Bacteria, or AOB) and a single lineage of archaea belonging to the Nitrosophaeria class of Thermoproteota (Ammonia Oxidizing Archaea, or AOA). Most cultivated AOA originate from marine or soil environments, but this may capture only a limited subset of the full diversity of this clade. Here, we describe several genomes of AOA from metagenomic sequencing of a hot spring microbial mat, representing several poorly characterized basal lineages that may be important for understanding the early evolution of archaeal ammonia oxidation. These genomes include a novel genus most closely related to Nitrososphaera as well as novel species belonging to the genera Nitrosotenuis, Nitrososphaera, and Nitrosotalea. Furthermore, the distributions and phylogenetic relationships of key metabolic genes support a history of vertical inheritance of ammonia oxidation and carbon fixation from the last common ancestor of crown group AOA.
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Please consider the points raised by the reviewers, overall it seems that you need the manuscript would benefit emphasizing its contributions compared to the current knowledge and clarify the taxonomy applied and use one consistently throughout the manuscript. Reviewer 2 has raised a number of specific points in addition that I would like you to address as well.
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Comments to Author
Dear Authors, I think that it is great to have new genomes of ammonia oxidizing archaea and I appreciate the time you took to investigate these genomes that came from a larger dataset. I would encourage you to consider the following points: 1.) There is a mix of taxonomies throughout the paper that make it difficult to follow. While the genomes were classified using GTDB, there are several references to the NCBI taxonomy, including the use of Thaumarchaeota in the title. This can lead to a good deal of confusion. For example, the GTDB order Nitrososphaerales encompasses all known AOA in the Thermoproteota phylum, but the NCBI order Nitrososphaerales (within the Thaumarchaeota phylum) only includes the soil lineages, with the additional orders of Nitrosopumilales, Nitrosotaleales, and …
Comments to Author
Dear Authors, I think that it is great to have new genomes of ammonia oxidizing archaea and I appreciate the time you took to investigate these genomes that came from a larger dataset. I would encourage you to consider the following points: 1.) There is a mix of taxonomies throughout the paper that make it difficult to follow. While the genomes were classified using GTDB, there are several references to the NCBI taxonomy, including the use of Thaumarchaeota in the title. This can lead to a good deal of confusion. For example, the GTDB order Nitrososphaerales encompasses all known AOA in the Thermoproteota phylum, but the NCBI order Nitrososphaerales (within the Thaumarchaeota phylum) only includes the soil lineages, with the additional orders of Nitrosopumilales, Nitrosotaleales, and Nitrososcaldales encompassing marine, acidic soil, and thermophilic lineages respectively. I would strongly encourage that you stick with one taxonomy throughout (likely GTDB). I also suspect that the title is meant to cover the class Nitrosospheria in Thaumarchaeota as Nitrososphaera is a genus and the discussed genomes cover more than the genus Nitrososphaera. In your introduction, I would also encourage you to state which taxonomy you are using throughout the paper. 2.) Having more genomes from a hot spring environment is of course beneficial. I would like to see the genomes put into the context of Luo et al. (https://doi.org/10.3389/fmicb.2020.608832) that also recovered several AOA genomes from hot springs. As the focus is on AOA from hot springs, I think this is an important missing reference. I.e., were the sampled hot springs similar/different? 3.) I find it very intriguing that no AMO or aerobic respiration sequences were found for NZW_233. I suspect this is due to missing contigs (as addressed in the manuscript). If not, it would be a significant finding. To investigate this further, have you compared the synteny of the collected contigs to other Nitrosospheara genomes? The synteny is strikingly similar between N. gargensis, N. viennensis, and Ca. N. evergladensis. Comparing the coverage you found to these genomes could be informative for these genes. The MAGE platform is a great tool for this (mage.genoscope.cns.fr). 4.) I found it surprising that there was no mention of the putative additional AMO subunits found in archaea (AmoXYZ, ref https://doi.org/10.1038/s41396-023-01367-3). This is a marked difference between the two domains. Is there a reason that these were excluded from the analysis? As they are mostly transmembrane helices, they might not contribute as much to the phylogenetic signal, but it would be nice to acknowledge this difference and an explanation for why they were or were not included. 5.) In lines 33-34 there is a nice example of the differences in AOA and AOB following the AMO step. It might also be worth noting differences at the step of the ammonia monooxygenase. For example, the apparent Km for ammonia is very different among these groups of ammonia oxidizers. See Jung et al., 2022(https://doi.org/10.1038/s41396-021-01064-z) and Kits et al., 2017 (https://doi-org.uaccess.univie.ac.at/10.1038/nature23679). This, along with the differences in AMO subunits would strengthen your discussion of the differences in AOA and AOB. 6.) From the methods, the samples were collected along a transect with a range of temperatures and a fluid pH of 8. It would be great to have this additional information for the genomes shown in Figure 1. For example, NZW_1495 is clearly in the thermophilic clade, while the rest are not. Is this explainable by temperature differences? Similarly, NZW_1382 is clearly grouping with acidic AOA strains. Does the pH for the sample where this genome was recovered from reflect that? Adding pH and temp measurements for the samples that the respective genomes came from in Figure 1 would go a long ways to put these genomes into the context of what is already known about the clades they are grouping with and would be of interest to the readers. Overall, I think the story is succinct and provides new AOA genomes. My biggest critique is to use a uniform taxonomy throughout the paper and pay close attention to the spelling of taxonomic clades. I would like to emphasize that this is the reason I have indicated the quality as "poor". However, this can easily be fixed and would benefit the overall story. I would also encourage the authors to cite recent literature of AOA from hot springs and relevant AMO differences between AOA and AOB. Specific comments can be found below: Title: If sticking with GTDB taxonomy, perhaps revise the title to "Novel Hot Spring Nitrososphearales support vertical inheritance of ammonia oxidation & carbon fixation in Thermoproteotoa" Line 17: "Nitrosphaera", is likely meant to be Nitrososphaera Line 28: change "until more" to "until a more" Line 30: Nitrososphaera is a genus, the class is Nitrososphaeria Line 43: Italicize Candidatus. This may depend on journal requirements as this is an order.
Please rate the manuscript for methodological rigour
Good
Please rate the quality of the presentation and structure of the manuscript
Poor
To what extent are the conclusions supported by the data?
Strongly support
Do you have any concerns of possible image manipulation, plagiarism or any other unethical practices?
No
Is there a potential financial or other conflict of interest between yourself and the author(s)?
No
If this manuscript involves human and/or animal work, have the subjects been treated in an ethical manner and the authors complied with the appropriate guidelines?
Yes
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Comments to Author
The manuscript presents metagenomic data on ammonia-oxidizing archaea (AOA) from hot spring microbial mats, and 7 MAGs predicted to be affiliated to the Nitrososphaeria class. The new MAGs contribute to our understanding of the evolution and diversity of archaeal ammonia oxidation. However, I recommend the authors clarify how their study provides novel contributions beyond what has already been established. For example, in 2007, Nitrososphaera gargensis was identified from a hot spring sample as an ammonia oxidizer, providing early insights into AOA diversity in similar environments. "A moderately thermophilic ammonia-oxidizing crenarchaeote from a hot spring" has also reported new species in the Nitrososphaera cluster. The manuscript may highlight the unique aspects of the genomes or metabolic …
Comments to Author
The manuscript presents metagenomic data on ammonia-oxidizing archaea (AOA) from hot spring microbial mats, and 7 MAGs predicted to be affiliated to the Nitrososphaeria class. The new MAGs contribute to our understanding of the evolution and diversity of archaeal ammonia oxidation. However, I recommend the authors clarify how their study provides novel contributions beyond what has already been established. For example, in 2007, Nitrososphaera gargensis was identified from a hot spring sample as an ammonia oxidizer, providing early insights into AOA diversity in similar environments. "A moderately thermophilic ammonia-oxidizing crenarchaeote from a hot spring" has also reported new species in the Nitrososphaera cluster. The manuscript may highlight the unique aspects of the genomes or metabolic pathways that distinguish this work from earlier research, particularly in relation to newly assembled MAGs in other studies.
Please rate the manuscript for methodological rigour
Good
Please rate the quality of the presentation and structure of the manuscript
Satisfactory
To what extent are the conclusions supported by the data?
Partially support
Do you have any concerns of possible image manipulation, plagiarism or any other unethical practices?
No
Is there a potential financial or other conflict of interest between yourself and the author(s)?
No
If this manuscript involves human and/or animal work, have the subjects been treated in an ethical manner and the authors complied with the appropriate guidelines?
Yes
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