The DOI matches its Crossref record; 1 of the 1 references it cites were found in a registry or an index.
Ultrahigh-affinity transport proteins from ubiquitous marine bacteria reveal mechanisms and global patterns of nutrient uptake
Open accessPreprint — published as 10.1038/s41586-024-07924-w · Paper page
Abstract
SAR11 bacteria are the most abundant members of the global ocean microbiome and have a broad impact on ocean ecosystems. To thrive in their competitive oligotrophic environments, these bacteria rely on solute-binding proteins (SBPs) that facilitate nutrient uptake through ABC transporters. Nonetheless, previous studies have been unable to access the molecular mechanisms and functions of these transporters because they rely heavily on homology-based predictions. These mechanisms and functions are essential to understand biogeochemical cycling in the ocean, including assimilation of dissolved organic matter (DOM). Here, by doing a biochemical study of the collective behavior of all SBPs in a SAR11 bacterium, we discover that these transporters have unprecedented binding affinity ( K d ≥30 pM) and unexpectedly high binding specificity, revealing molecular mechanisms for oligotrophic adaptation. Our study uncovers new carbon sources for the SAR11 bacteria and provides an accurate biogeographical map of nutrient uptake in the ocean. Our results show how functional adaptation at the molecular level in ubiquitous marine bacteria impacts global patterns of DOM assimilation and provides insight into the contribution of different compounds to oceanic nutrient cycles.
Overview
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Citations
Cites
Highly accurate protein structure prediction with AlphaFold
Jumper, J., Evans, R., Pritzel, A., Green, T., Figurnov, M., Ronneberger, O., Tunyasuvunakool, K., Bates, R., Žídek, A., Potapenko, A., et al. (2021) · Nature · doi:10.1038/s41586-021-03819-2 · Cited by 43,764
Flagged first, then by citations
Research works printed but not linked: 82
- 10.1146/annurev-marine-010814-015934 · DOI
- 10.1038/nature01240 · DOI · Paper page
- 10.1111/j.1462-2920.2009.01929.x · DOI
- 10.1126/science.1114057 · DOI
- 10.1111/j.1462-2920.2008.01758.x · DOI
- 10.1038/nature06776 · DOI
- 10.1038/ncomms5346 · DOI
- 10.1128/AEM.70.7.4129-4135.2004 · DOI
- 10.1128/AEM.71.6.2979-2986.2005 · DOI
- 10.1007/s00248-019-01320-y · DOI
- 2016, The abundant marine bacterium Pelagibacter simultaneously catabolizes dimethylsulfoniopropionate to the gases dimethyl sulfide and methanethiol, Nat. Microbiol., 1, 16065, 10.1038/nmicrobiol.2016.65 · DOI
- 10.1128/AEM.05640-11 · DOI
- 2022, Microbial metabolites in the marine carbon cycle, Nat. Microbiol., 7, 508, 10.1038/s41564-022-01090-3 · DOI
- 2021, Selective nutrient transport in bacteria: multicomponent transporter systems reign supreme, Front. Mol. Biosci., 8, 699222, 10.3389/fmolb.2021.699222 · DOI
- 10.1016/j.febslet.2010.04.043 · DOI
- 10.1128/AEM.00599-08 · DOI
- 10.1038/ismej.2008.83 · DOI
- 10.1371/journal.pcbi.1000605 · DOI
- 10.1101/2023.01.19.524783 · DOI
- 10.1111/1462-2920.14649 · DOI
- 10.1038/s41396-023-01375-3 · DOI
- 10.1128/MMBR.00031-07 · DOI
- 10.1021/bi501388y · DOI
- 2018, Functional assignment of multiple catabolic pathways for D-apiose, Nat. Chem. Biol., 14, 696, 10.1038/s41589-018-0067-7 · DOI
- 10.1038/ismej.2014.61 · DOI
- 2019, Sulfonate-based networks between eukaryotic phytoplankton and heterotrophic bacteria in the surface ocean, Nat. Microbiol., 4, 1706, 10.1038/s41564-019-0507-5 · DOI
- 10.1038/ismej.2012.122 · DOI
- 2011, One carbon metabolism in SAR11 pelagic marine bacteria, PLoS One, 6, 23973, 10.1371/journal.pone.0023973 · DOI
- 10.1007/978-1-4939-7577-8_23 · DOI
- 10.1038/s41589-018-0043-2 · DOI
- 2022, Characterization of the trimethylamine N-oxide transporter from Pelagibacter strain HTCC1062 reveals its oligotrophic niche adaption, Front. Microbiol., 13, 838608, 10.3389/fmicb.2022.838608 · DOI
- 10.1006/abio.1999.4402 · DOI
- 2022, The Ocean Gene Atlas v2.0: online exploration of the biogeography and phylogeny of plankton genes, Nucleic Acids Res., 50, W516, 10.1093/nar/gkac420 · DOI
- 10.1038/ngeo1765 · DOI · Paper page
- 10.1126/science.abe6301 · DOI
- 2021, SAR11 cells rely on enzyme multifunctionality to metabolize a range of polyamine compounds, MBio, 12, 0109121
- 10.1371/journal.pone.0019725 · DOI
- 2013, Proteomic and transcriptomic analyses of “Candidatus Pelagibacter ubique” describe the first PII-independent response to nitrogen limitation in a free-living Alphaproteobacterium, MBio, 4, e00133
- Smith, D. P. et al. Proteome remodeling in response to sulfur limitation in “Candidatus Pelagibacter ubique”. mSystems 1, (2016). · DOI
- 10.1007/s12275-013-2671-2 · DOI
- 10.3354/meps070189 · DOI
- 2007, Differential microbial uptake of dissolved amino acids and amino sugars in surface waters of the Atlantic Ocean, J. Plankton Res., 30, 211, 10.1093/plankt/fbm091 · DOI
- 2017, Crustacean zooplankton release copious amounts of dissolved organic matter as taurine in the ocean, Limnol. Oceanogr., 62, 2745, 10.1002/lno.10603 · DOI
- 1998, Glycine betaine uptake, retention, and degradation by microorganisms in seawater, Limnol. Oceanogr., 43, 1592, 10.4319/lo.1998.43.7.1592 · DOI
- 2021, Mechanistic model of nutrient uptake explains dichotomy between marine oligotrophic and copiotrophic bacteria, PLoS Comput. Biol., 17, e1009023, 10.1371/journal.pcbi.1009023 · DOI
- 2020, Accumulation of ambient phosphate into the periplasm of marine bacteria is proton motive force dependent, Nat. Commun., 11, 2642, 10.1038/s41467-020-16428-w · DOI
- 10.1128/AEM.02807-16 · DOI
- 2015, Dominant oceanic bacteria secure phosphate using a large extracellular buffer, Nat. Commun., 6, 7878, 10.1038/ncomms8878 · DOI
- 10.1038/nature11517 · DOI
- 2022, Standardized multi-omics of Earth’s microbiomes reveals microbial and metabolite diversity, Nat. Microbiol., 7, 2128, 10.1038/s41564-022-01266-x · DOI
- 10.1038/nature06810 · DOI · Paper page
- 10.1126/science.aaf4507 · DOI
- 2021, Functional characterisation of substrate-binding proteins to address nutrient uptake in marine picocyanobacteria, Biochem. Soc. Trans., 49, 2465, 10.1042/BST20200244 · DOI
- 10.1093/nar/gkw1068 · DOI
- 10.1038/s41587-019-0036-z · DOI
- 10.1016/j.pep.2006.09.015 · DOI
- 2015, An efficient protocol to enhance recombinant protein expression using ethanol in Escherichia coli, MethodsX, 2, 385, 10.1016/j.mex.2015.09.005 · DOI
- 2016, Ancestral protein reconstruction yields insights into adaptive evolution of binding specificity in solute-binding proteins, Cell Chem. Biol., 23, 236, 10.1016/j.chembiol.2015.12.010 · DOI
- 10.1111/mmi.12964 · DOI
- 2018, Screening chemoreceptor-ligand interactions by high-throughput thermal-shift assays, Methods Mol. Biol., 1729, 281, 10.1007/978-1-4939-7577-8_22 · DOI
- 10.1021/acs.biochem.7b01264 · DOI
- 10.1038/nprot.2006.28 · DOI
- 10.1074/jbc.M709907200 · DOI
- 10.1074/jbc.M704136200 · DOI
- 10.1111/j.1365-2958.1993.tb01957.x · DOI
- 10.1107/S2059798318017795 · DOI
- 10.1107/S0907444909047337 · DOI · Paper page
- 2018, KAMO: towards automated data processing for microcrystals, Acta Crystallogr. D Struct. Biol., 74, 441, 10.1107/S2059798318004576 · DOI
- 2022, ColabFold: making protein folding accessible to all, Nat. Methods, 19, 679, 10.1038/s41592-022-01488-1 · DOI · Paper page
- 10.1107/S0021889807021206 · DOI · Paper page
- 10.1107/S0021889897006766 · DOI
- 10.1107/S0907444996012255 · DOI
- 10.1107/S2059798319011471 · DOI · Paper page
- 10.1107/S0907444904019158 · DOI · Paper page
- UniProt Consortium, 2023, Uniprot: the universal protein knowledgebase in 2023, Nucleic Acids Res., 51, D523, 10.1093/nar/gkac1052 · DOI · Paper page
- 10.1093/nar/gkh340 · DOI · Paper page
- 10.1093/bioinformatics/btp348 · DOI
- 10.1371/journal.pone.0009490 · DOI · Paper page
- 10.1093/NAR/GKAB1061 · DOI · Paper page
- 2016, ggtree: An R package for visualization and annotation of phylogenetic trees with their covariates and other associated data, Methods Ecol. Evol., 8, 28
- 10.1111/j.1462-2920.2009.02092.x · DOI
- 10.1073/pnas.1317834111 · DOI · Paper page
Metadata
- Authors
- Clifton, B. E., Alcolombri, U., Jackson, C. J., & Laurino, P.
- Affiliations
- Okinawa Institute of Science and Technology Graduate University (JP)
- Hebrew University of Jerusalem (IL)
- Australian National University (AU)
- Corresponding author
- Clifton, Ben E.
- Laurino, Paola
- Venue
- Nature
- Publisher
- openRxiv
- Published
- 2023-02-16
- Volume
- 634
- Issue
- 8034
- Pages
- 721-728
- ISSN
- 0028-0836 (ISSN-L)
- PMC
- PMC11485210
- OpenAlex
- W4402437897
- Cited by
- 37
- References
- 1
- Citations by year
- 2026: 16 · 2025: 18 · 2024: 3
- FWCI
- 10.15
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- cc-by-nc-nd
- Locations
- Nature (publishedVersion, cc-by-nc-nd)
- bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nc-nd)
- PubMed Central (publishedVersion, cc-by-nc-nd)
- PubMed (publishedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- Institutional Repositories DataBase (IRDB) (submittedVersion)
- Okinawa Institute of Science and Technology Graduate University (Okinawa Institute of Science and Technology Graduate University) (submittedVersion, cc-by-nc-nd)
- ANU Open Research (Australian National University) (submittedVersion)
- Funders
- Okinawa Institute of Science and Technology Graduate University
- Japan Society for the Promotion of Science
- Topics
- Physical Sciences › Environmental Science › Ecology › Microbial Community Ecology and Physiology
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
- Physical Sciences › Earth and Planetary Sciences › Oceanography › Marine Plankton and Biogeochemistry
- Keywords
- solute binding protein, membrane transporters, substrate uptake, binding specificity, marine bacteria, carbon source, biogeochemical cycles, genome-wide characterization
- MeSH terms
- Bacteria, Bacterial Proteins, Carbon, Carrier Proteins, Oceans and Seas, Organic Chemicals, Protein Binding, Seawater, Substrate Specificity, Genome, Bacterial, Membrane Transport Proteins, Phylogeography, Aquatic Organisms
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
