High genetic diversity in the pelagic deep-sea fauna of the Atacama Trench revealed by environmental DNA
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Curated by eLife
eLife assessment
This manuscript from Ramírez-Flandes will be of interest to marine biologists, deep ocean ecologists, conservation biologists, and biogeographers. At times, the comparison of merely a pair of samples or sampling locales can substantially widen our view of biological and ecological systems and processes. In the case of this study, the pattern of metazoan diversity from eDNA samples from across the water columns in comparable series from two deep trench systems (to below 8000 m) is markedly different, including evidence of substantial biological diversity deep in the Atacama Trench (to a much greater extent than observed in the Kermadec Trench), contradicting existing paradigms about biodiversity potential in abyssal-hadal regions.
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- Ecology (eLife)
Abstract
A current paradigm in marine biodiversity states that faunal richness decreases with depth. However, the deep-ocean ecosystem has been significantly under-sampled, hindering a complete view of its biodiversity. This situation is accentuated in ultra-deep waters, where the remote and extreme conditions unfit the traditional sampling methods. Using environmental DNA, we assessed the pelagic metazoan diversity of the Atacama Trench from the high-productive near-surface level down to ~8000 m depth. Our results show that waters deeper than 4000 m contributed up to 50% of the overall genetic diversity. These findings contrast with similar observations in the less-productive Kermadec Trench, where the diversity in deep waters was lower than in shallower waters. Moreover, both deep pelagic ecosystems exhibited some unknown phylogenetic clades within the dominant taxonomic groups: hydrozoans and copepods. The deep-ocean biota may thus contribute to global biodiversity far more than hitherto suggested, especially in zones influenced by high primary production. Our results underline the need for increased effort to study these remote ecosystems and improve our understanding of their contribution to the ecology and biogeochemistry of the deep-sea pelagic and benthic realms.
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Author Response
Reviewer #1 (Public Review):
While eDNA methods are becoming more established, there remains skepticism by many in the scientific community about the origins of the detected DNA (e.g. does it drift in from other areas or water layers?). If these concerns aren't addressed (i.e. by citing supporting literature on the fate of eDNA), the different biodiversity profiles between trenches could possibly be explained by differing oceanography. There is also some important methodological information that is missing from this manuscript. For example, sampling volumes will affect the amount of biodiversity detected, but it is not clear if sample volumes are consistent across depths and study areas. It was also not indicated whether field controls (blanks) were taken to assess the potential contamination of samples. Lastly, the …
Author Response
Reviewer #1 (Public Review):
While eDNA methods are becoming more established, there remains skepticism by many in the scientific community about the origins of the detected DNA (e.g. does it drift in from other areas or water layers?). If these concerns aren't addressed (i.e. by citing supporting literature on the fate of eDNA), the different biodiversity profiles between trenches could possibly be explained by differing oceanography. There is also some important methodological information that is missing from this manuscript. For example, sampling volumes will affect the amount of biodiversity detected, but it is not clear if sample volumes are consistent across depths and study areas. It was also not indicated whether field controls (blanks) were taken to assess the potential contamination of samples. Lastly, the literature in the eDNA field is progressing rapidly and there are some missing papers (e.g Thomsen et al. 2016, Canals et al. 2021, McClenaghan et al. 2020, Govindarajan et al. 2021, etc.) that are relevant to the technique used in this manuscript and the habitat studied.
We are very grateful to this reviewer for providing such an in-depth review of our manuscript that allowed us to improve our manuscript significantly. We tried to follow explicitly almost every suggestion. In particular, we appreciate the input of other important missing literature that we readily included in this new version of our paper. The data on the volume of seawater filtered for each sample is given in Table Supplementary file 1a. Regarding field blanks, they were not collected per se. However, as part of the molecular protocol used (see Methodology) a “negative extraction control” was applied to check for possible contamination. Also, from the results themselves, we carefully checked for any indication of contamination that could have biased our results and conclusions.
Reviewer #2 (Public Review):
My primary critique is the near-absence of statistical analyses in the current version of the manuscript that are necessary to support the many descriptive observations made with a more formal hypothesis testing framework, as well. Developing an appropriate framework for such analyses throughout the paper, including consideration of the multiple tests that will be performed. This is important for many reasons, including by providing a more formal sense of uncertainty in the conclusions to readers, given the understandable sampling limitations. Planning and conducting these analyses will require considerable work.
We thank the reviewer for raising such concern. We did include statistical analyses in part of our work. For example, all the phylogenetic analyses (using the IQ-tree software) implicitly include statistical analyses. The calculation of the Gini index in Figure 2 is also a statistical measure. However, we agree with the reviewer that some of our results lacked statistical analysis. We thus now include statistical significance to more statements in the text and additional panels to Figure S2—figure supplement 1 (with support on data in new tables in Supplementary file 1h and 1i) to illustrate the statistical support to some of our claims. We have also removed some unnecessary statement.
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eLife assessment
This manuscript from Ramírez-Flandes will be of interest to marine biologists, deep ocean ecologists, conservation biologists, and biogeographers. At times, the comparison of merely a pair of samples or sampling locales can substantially widen our view of biological and ecological systems and processes. In the case of this study, the pattern of metazoan diversity from eDNA samples from across the water columns in comparable series from two deep trench systems (to below 8000 m) is markedly different, including evidence of substantial biological diversity deep in the Atacama Trench (to a much greater extent than observed in the Kermadec Trench), contradicting existing paradigms about biodiversity potential in abyssal-hadal regions.
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Reviewer #1 (Public Review):
The authors of this paper have used emerging environmental DNA (eDNA) methods to profile depth-biodiversity in two deep ocean trenches.
Strengths:
Working in deep ocean habitats is challenging and this paper provides data from not one but two deep ocean trenches and provides new perspectives on biodiversity distributions in these habitats. The most interesting finding is that deep ocean habitats appear to contribute much more biodiversity, as measured using relatively novel eDNA techniques than previously thought. The comparison of these two trenches also illustrates the variable nature of these biodiversity patterns and suggests trench-specific features (e.g. unique habitats and/or productivity) influence deep ocean biodiversity.Weaknesses:
While eDNA methods are becoming more established, there remains …Reviewer #1 (Public Review):
The authors of this paper have used emerging environmental DNA (eDNA) methods to profile depth-biodiversity in two deep ocean trenches.
Strengths:
Working in deep ocean habitats is challenging and this paper provides data from not one but two deep ocean trenches and provides new perspectives on biodiversity distributions in these habitats. The most interesting finding is that deep ocean habitats appear to contribute much more biodiversity, as measured using relatively novel eDNA techniques than previously thought. The comparison of these two trenches also illustrates the variable nature of these biodiversity patterns and suggests trench-specific features (e.g. unique habitats and/or productivity) influence deep ocean biodiversity.Weaknesses:
While eDNA methods are becoming more established, there remains skepticism by many in the scientific community about the origins of the detected DNA (e.g. does it drift in from other areas or water layers?). If these concerns aren't addressed (i.e. by citing supporting literature on the fate of eDNA), the different biodiversity profiles between trenches could possibly be explained by differing oceanography. There is also some important methodological information that is missing from this manuscript. For example, sampling volumes will affect the amount of biodiversity detected, but it is not clear if sample volumes are consistent across depths and study areas. It was also not indicated whether field controls (blanks) were taken to assess the potential contamination of samples. Lastly, the literature in the eDNA field is progressing rapidly and there are some missing papers (e.g Thomsen et al. 2016, Canals et al. 2021, McClenaghan et al. 2020, Govindarajan et al. 2021, etc.) that are relevant to the technique used in this manuscript and the habitat studied. -
Reviewer #2 (Public Review):
I found the study and findings important and largely convincing. While some of these observations might continue to refine with further sampling, the value of these data for what they already are, the novelty in the comparison, and the strength and importance of these results for our understanding of deep-sea marine ecosystems and variation thereof, are all exemplary.
My primary critique is the near-absence of statistical analyses in the current version of the manuscript that are necessary to support the many descriptive observations made with a more formal hypothesis testing framework, as well. Developing an appropriate framework for such analyses throughout the paper, including consideration of the multiple tests that will be performed. This is important for many reasons, including by providing a more …
Reviewer #2 (Public Review):
I found the study and findings important and largely convincing. While some of these observations might continue to refine with further sampling, the value of these data for what they already are, the novelty in the comparison, and the strength and importance of these results for our understanding of deep-sea marine ecosystems and variation thereof, are all exemplary.
My primary critique is the near-absence of statistical analyses in the current version of the manuscript that are necessary to support the many descriptive observations made with a more formal hypothesis testing framework, as well. Developing an appropriate framework for such analyses throughout the paper, including consideration of the multiple tests that will be performed. This is important for many reasons, including by providing a more formal sense of uncertainty in the conclusions to readers, given the understandable sampling limitations. Planning and conducting these analyses will require considerable work.
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