Diagnosing nutritional stress in the oceans

doi:10.1126/science.abi4684

GSTDTAP > 气候变化

DOI	10.1126/science.abi4684
	Diagnosing nutritional stress in the oceans
	Maureen Coleman
	2021-04-16
发表期刊	Science
出版年	2021
英文摘要	Marine phytoplankton perform almost half of global photosynthesis, and their capacity for carbon uptake is governed by the availability of scarce nutrients. Climate change and anthropogenic inputs are altering the oceanic distribution of these nutrients ([ 1 ][1], [ 2 ][2]). How individual phytoplankton groups and ocean productivity are responding to these changes is unknown. On page 287 of this issue, Ustick et al. ([ 3 ][3]) present a global map of nutrient limitation in Prochlorococcus , the most abundant photosynthetic organism in the low-latitude oceans, on the basis of a new diagnostic metric that could be widely used to monitor shifts in the nutritional seascape. The classical test for limitation is a nutrient-amendment experiment: Phytoplankton growth rate and/or biomass increase when the limiting nutrient is added but remain unaffected by other supplements. This approach has long been used in small-scale incubations and whole-ecosystem manipulations, proving that phosphorus controls algal biomass in lakes ([ 4 ][4]) and that iron limits phytoplankton growth in so-called high-nitrate low-chlorophyll ocean regions ([ 5 ][5]). Geochemists also infer nutrient deficiency by comparing ratios of dissolved nutrients to the Redfield stoichiometry (the average ratio of carbon, nitrogen, and phosphorus found in marine phytoplankton biomass). Molecular approaches assay the physiological state of cells using RNA or protein expression ([ 6 ][6], [ 7 ][7]). Yet, all these approaches are low-throughput and laborious, requiring meticulous precautions to prevent trace-metal contamination and exacting analytical methods for low-level detection. By contrast, the metric developed by Ustick et al. requires only routine sampling and DNA sequencing of microbial communities, a common approach to survey taxonomic composition and functional potential ([ 8 ][8]). But the authors extract new information by simplifying complex metagenomes down to a single taxon, Prochlorococcus. Prochlorococcus genomes continually gain and lose genes, and “use it or lose it” dictates whether a gene persists. Genes that enhance fitness—for instance, by increasing the rate at which a growth-limiting nutrient can be transported into the cell—are selectively retained in genomes. Ultimately, every cell in the population may carry the beneficial gene through a combination of vertical inheritance and horizontal gene transfer. Hence, the frequency of the gene, relative to the average core housekeeping gene, serves as a proxy for the physiological limitation that the gene product relieves. ![Figure][9] Gene frequencies as a biosensor for ocean nutrient limitation The phytoplankton Prochlorococcus adapts to local environments by gene gain and loss. Dashed arrows show cells that are outcompeted for the limiting nutrient, leading to gene loss from the population. HGT, horizontal gene transfer; DOP, dissolved organic phosphorus. GRAPHIC: N. DESAI/ SCIENCE Ustick et al. propose a set of diagnostic genes that are linked to phosphorus, nitrogen, or iron stress in Prochlorococcus (see the figure). The authors then quantify the frequency of these genes in more than a thousand samples—the vast majority newly collected and sequenced. Their metric confirms results from well-characterized locations (e.g., phosphorus limitation in the North Atlantic gyre) ([ 9 ][10]) while also revealing the stress “felt” by Prochlorococcus in uncharted regions of the Indian Ocean. In the Atlantic, criss-crossing cruise tracks spanning 50°S to 50°N latitude mapped sharp transitions between regions of phosphorus, nitrogen, and iron limitation. Notably, the distributions of marker genes for multiple stressors sometimes overlapped, suggesting the potential for widespread colimitation, or the mixing of populations with distinct nutritional histories. The elegant simplicity of this genetic approach belies many underlying uncertainties. One key mystery is the major mode and rates of gene acquisition by Prochlorococcus cells. Studies have pointed to viruses ([ 10 ][11]) and membrane vesicles ([ 11 ][12]) and potentially to mobile genetic elements ([ 12 ][13]) as playing roles. To increase the sensitivity of the new metric, Ustick et al. categorized each diagnostic gene by the severity of stress (high, medium, or low) it indicates—for example, alkaline phosphatase is presumed to persist only under the most severe phosphorus stress—but the biochemical trade-offs that underpin these categories have not been characterized and likely differ across taxa. How generalizable this approach is to other taxa remains to be seen. More generally, what does this approach, and the resulting map of globalscale nutrient stress, reveal about ocean biogeochemistry and controls on carbon uptake? Ustick et al. suggest that their genetic approach is validated by its consistency with classical nutrient amendment experiments. However, there are also discrepancies between the approaches, which is not unexpected and is intriguing. Experiments typically measure the short-term response to nutrient addition in terms of community-level biomass or carbon uptake. The gene metrics used here assess the impact of natural selection, integrated over unspecified time and space, on a single organism. Relating the two measures is not straightforward. Adding back the genome-reported limiting nutrient would not necessarily increase the growth rate or biomass of Prochlorococcus , whose growth rate would likely already be near maximal. But it could still increase community-level biomass and carbon uptake by replacing Prochlorococcus with faster-growing, larger taxa. These newly abundant taxa would have distinct stoichiometric requirements compared with Prochlorococcus , and thus their growth might be limited by different nutrients. Teasing apart the reasons why individual taxa and the community as a whole respond differently to nutrient amendments could provide important new insights into the physiological and ecological controls imposed by nutrient limitation. The atlas of nutrient limitation presented by Ustick et al. leverages routine metagenomic samples collected on a massive scale, providing a baseline assessment of global Prochlorococcus nutritional status. Using this approach over time promises to document changing pressures felt by Prochlorococcus and potentially other taxa. It will not replace field experiments, physiology, and geochemical tools but rather will complement these approaches with its extremely sensitive and taxon-specific readout. By integrating multiple methods and understanding their (dis)agreements, scientists will be better equipped to monitor, and forecast, changes in ocean biogeochemistry and carbon uptake. 1. [↵][14]1. C. M. Moore et al ., Nat. Geosci. 6, 701 (2013). [OpenUrl][15][CrossRef][16][GeoRef][17] 2. [↵][18]1. A. Krishnamurthy et al ., Global Biogeochem. Cycles 23, GB3016 (2009). [OpenUrl][19][CrossRef][20] 3. [↵][21]1. L. J. Ustick et al ., Science 372, 287 (2021). [OpenUrl][22][Abstract/FREE Full Text][23] 4. [↵][24]1. D. W. Schindler , Science 184, 897 (1974). [OpenUrl][25][Abstract/FREE Full Text][26] 5. [↵][27]1. K. H. Coale et al ., Nature 383, 495 (1996). [OpenUrl][28][CrossRef][29][GeoRef][30][PubMed][31][Web of Science][32] 6. [↵][33]1. A. Marchetti et al ., Proc. Natl. Acad. Sci. U.S.A. 109, E317 (2012). [OpenUrl][34][Abstract/FREE Full Text][35] 7. [↵][36]1. M. A. Saito , c Science 345, 1173 (2014). [OpenUrl][37] 8. [↵][38]1. S. Sunagawa et al ., Science 348, 1261359 (2015). [OpenUrl][39][Abstract/FREE Full Text][40] 9. [↵][41]1. M. L. Coleman, 2. S. W. Chisholm , Proc. Natl. Acad. Sci. U.S.A. 107, 18634 (2010). [OpenUrl][42][Abstract/FREE Full Text][43] 10. [↵][44]1. R. Laurenceau et al ., ISME J. 15, 129 (2021). [OpenUrl][45] 11. [↵][46]1. S. J. Biller et al ., Science 343, 183 (2014). [OpenUrl][47][Abstract/FREE Full Text][48] 12. [↵][49]1. T. Hackl et al ., bioRxiv 10.1101/2020.12.28.424599 (2020). [1]: #ref-1 [2]: #ref-2 [3]: #ref-3 [4]: #ref-4 [5]: #ref-5 [6]: #ref-6 [7]: #ref-7 [8]: #ref-8 [9]: pending:yes [10]: #ref-9 [11]: #ref-10 [12]: #ref-11 [13]: #ref-12 [14]: #xref-ref-1-1 "View reference 1 in text" [15]: {openurl}?query=rft.stitle%253DNat%2BGeosci%26rft.aulast%253DMoore%26rft.auinit1%253DC.%2BM.%26rft.volume%253D6%26rft.issue%253D9%26rft.spage%253D701%26rft.epage%253D710%26rft.atitle%253DProcesses%2Band%2Bpatterns%2Bof%2Boceanic%2Bnutrient%2Blimitation%26rft_id%253Dinfo%253Adoi%252F10.1038%252Fngeo1765%26rft.genre%253Darticle%26rft_val_fmt%253Dinfo%253Aofi%252Ffmt%253Akev%253Amtx%253Ajournal%26ctx_ver%253DZ39.88-2004%26url_ver%253DZ39.88-2004%26url_ctx_fmt%253Dinfo%253Aofi%252Ffmt%253Akev%253Amtx%253Actx [16]: /lookup/external-ref?access_num=10.1038/ngeo1765&link_type=DOI [17]: /lookup/external-ref?access_num=2014021988&link_type=GEOREF [18]: #xref-ref-2-1 "View reference 2 in text" [19]: {openurl}?query=rft.jtitle%253DGlobal%2BBiogeochem.%2BCycles%26rft.volume%253D23%26rft.spage%253DGB3016%26rft_id%253Dinfo%253Adoi%252F10.1029%252F2008GB003440%26rft.genre%253Darticle%26rft_val_fmt%253Dinfo%253Aofi%252Ffmt%253Akev%253Amtx%253Ajournal%26ctx_ver%253DZ39.88-2004%26url_ver%253DZ39.88-2004%26url_ctx_fmt%253Dinfo%253Aofi%252Ffmt%253Akev%253Amtx%253Actx [20]: /lookup/external-ref?access_num=10.1029/2008GB003440&link_type=DOI [21]: #xref-ref-3-1 "View reference 3 in text" [22]: {openurl}?query=rft.jtitle%253DScience%26rft.stitle%253DScience%26rft.aulast%253DUstick%26rft.auinit1%253DL.%2BJ.%26rft.volume%253D372%26rft.issue%253D6539%26rft.spage%253D287%26rft.epage%253D291%26rft.atitle%253DMetagenomic%2Banalysis%2Breveals%2Bglobal-scale%2Bpatterns%2Bof%2Bocean%2Bnutrient%2Blimitation%26rft_id%253Dinfo%253Adoi%252F10.1126%252Fscience.abe6301%26rft.genre%253Darticle%26rft_val_fmt%253Dinfo%253Aofi%252Ffmt%253Akev%253Amtx%253Ajournal%26ctx_ver%253DZ39.88-2004%26url_ver%253DZ39.88-2004%26url_ctx_fmt%253Dinfo%253Aofi%252Ffmt%253Akev%253Amtx%253Actx [23]: /lookup/ijlink/YTozOntzOjQ6InBhdGgiO3M6MTQ6Ii9sb29rdXAvaWpsaW5rIjtzOjU6InF1ZXJ5IjthOjQ6e3M6ODoibGlua1R5cGUiO3M6NDoiQUJTVCI7czoxMToiam91cm5hbENvZGUiO3M6Mzoic2NpIjtzOjU6InJlc2lkIjtzOjEyOiIzNzIvNjUzOS8yODciO3M6NDoiYXRvbSI7czoyMjoiL3NjaS8zNzIvNjUzOS8yMzkuYXRvbSI7fXM6ODoiZnJhZ21lbnQiO3M6MDoiIjt9 [24]: #xref-ref-4-1 "View reference 4 in text" [25]: 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{openurl}?query=rft.jtitle%253Dc%2BScience%26rft.volume%253D345%26rft.spage%253D1173%26rft.genre%253Darticle%26rft_val_fmt%253Dinfo%253Aofi%252Ffmt%253Akev%253Amtx%253Ajournal%26ctx_ver%253DZ39.88-2004%26url_ver%253DZ39.88-2004%26url_ctx_fmt%253Dinfo%253Aofi%252Ffmt%253Akev%253Amtx%253Actx [38]: #xref-ref-8-1 "View reference 8 in text" [39]: {openurl}?query=rft.jtitle%253DScience%26rft.stitle%253DScience%26rft.aulast%253DSunagawa%26rft.auinit1%253DS.%26rft.volume%253D348%26rft.issue%253D6237%26rft.spage%253D1261359%26rft.epage%253D1261359%26rft.atitle%253DStructure%2Band%2Bfunction%2Bof%2Bthe%2Bglobal%2Bocean%2Bmicrobiome%26rft_id%253Dinfo%253Adoi%252F10.1126%252Fscience.1261359%26rft_id%253Dinfo%253Apmid%252F25999513%26rft.genre%253Darticle%26rft_val_fmt%253Dinfo%253Aofi%252Ffmt%253Akev%253Amtx%253Ajournal%26ctx_ver%253DZ39.88-2004%26url_ver%253DZ39.88-2004%26url_ctx_fmt%253Dinfo%253Aofi%252Ffmt%253Akev%253Amtx%253Actx [40]: /lookup/ijlink/YTozOntzOjQ6InBhdGgiO3M6MTQ6Ii9sb29rdXAvaWpsaW5rIjtzOjU6InF1ZXJ5IjthOjQ6e3M6ODoibGlua1R5cGUiO3M6NDoiQUJTVCI7czoxMToiam91cm5hbENvZGUiO3M6Mzoic2NpIjtzOjU6InJlc2lkIjtzOjE2OiIzNDgvNjIzNy8xMjYxMzU5IjtzOjQ6ImF0b20iO3M6MjI6Ii9zY2kvMzcyLzY1MzkvMjM5LmF0b20iO31zOjg6ImZyYWdtZW50IjtzOjA6IiI7fQ== [41]: #xref-ref-9-1 "View reference 9 in text" [42]: {openurl}?query=rft.jtitle%253DProc.%2BNatl.%2BAcad.%2BSci.%2BU.S.A.%26rft_id%253Dinfo%253Adoi%252F10.1073%252Fpnas.1009480107%26rft_id%253Dinfo%253Apmid%252F20937887%26rft.genre%253Darticle%26rft_val_fmt%253Dinfo%253Aofi%252Ffmt%253Akev%253Amtx%253Ajournal%26ctx_ver%253DZ39.88-2004%26url_ver%253DZ39.88-2004%26url_ctx_fmt%253Dinfo%253Aofi%252Ffmt%253Akev%253Amtx%253Actx [43]: 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{openurl}?query=rft.jtitle%253DScience%26rft.stitle%253DScience%26rft.aulast%253DBiller%26rft.auinit1%253DS.%2BJ.%26rft.volume%253D343%26rft.issue%253D6167%26rft.spage%253D183%26rft.epage%253D186%26rft.atitle%253DBacterial%2BVesicles%2Bin%2BMarine%2BEcosystems%26rft_id%253Dinfo%253Adoi%252F10.1126%252Fscience.1243457%26rft_id%253Dinfo%253Apmid%252F24408433%26rft.genre%253Darticle%26rft_val_fmt%253Dinfo%253Aofi%252Ffmt%253Akev%253Amtx%253Ajournal%26ctx_ver%253DZ39.88-2004%26url_ver%253DZ39.88-2004%26url_ctx_fmt%253Dinfo%253Aofi%252Ffmt%253Akev%253Amtx%253Actx [48]: /lookup/ijlink/YTozOntzOjQ6InBhdGgiO3M6MTQ6Ii9sb29rdXAvaWpsaW5rIjtzOjU6InF1ZXJ5IjthOjQ6e3M6ODoibGlua1R5cGUiO3M6NDoiQUJTVCI7czoxMToiam91cm5hbENvZGUiO3M6Mzoic2NpIjtzOjU6InJlc2lkIjtzOjEyOiIzNDMvNjE2Ny8xODMiO3M6NDoiYXRvbSI7czoyMjoiL3NjaS8zNzIvNjUzOS8yMzkuYXRvbSI7fXM6ODoiZnJhZ21lbnQiO3M6MDoiIjt9 [49]: #xref-ref-12-1 "View reference 12 in text"
领域	气候变化 ; 资源环境
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引用统计
文献类型	期刊论文
条目标识符	http://119.78.100.173/C666/handle/2XK7JSWQ/322886
专题	气候变化资源环境科学
推荐引用方式 GB/T 7714	Maureen Coleman. Diagnosing nutritional stress in the oceans[J]. Science,2021.
APA	Maureen Coleman.(2021).Diagnosing nutritional stress in the oceans.Science.
MLA	Maureen Coleman."Diagnosing nutritional stress in the oceans".Science (2021).