[en] One of Earth’s largest carbon fluxes is driven by particles made from photosynthetically fixed matter, which aggregate and sink into the deep ocean. While biodegradation is known to reduce this vertical flux, the biophysical processes that control particle sinking speed are not well understood. Here, we use a vertical millifluidic column to video-track single particles and find that biogels scavenged by particles during sinking significantly reduce the particles’ sinking speed, slowing them by up to 45% within one day. Combining observations with a mathematical model, we determine that the mechanism for this slowdown is a combination of increased drag due to the formation of biogel tendrils and increased buoyancy due to the biogel’s low density. Because biogels are pervasive in the ocean, we propose that by slowing the sinking of organic particles they attenuate the vertical carbon flux in the ocean.
FNR13719464 - TOPOFLUME - Topological Fluid Mechanics: Decoding Emergent Dynamics In Anisotropic Fluids And Living Systems, 2019 (01/09/2020-31/08/2023) - Anupam Sengupta
Name of the research project :
R-AGR-3401 - A17/MS/11572821/MBRACE - part UL - SENGUPTA Anupam
Funders :
FNR - Fonds National de la Recherche Human Frontier Science Program EMBO - European Molecular Biology Organization Marie Skłodowska-Curie Actions SNSF - Swiss National Science Foundation Gordon and Betty Moore Foundation Simons Foundation
Funding number :
ATTRACT Grant no. A17/MS/11572821/MBRACE; CORE Grant no. C19/MS/13719464/TOPOFLUME/Sengupta; EMBO ALTF 1109-2016; HFSP LT001209/2017; Marie Skłodowska-Curie grant agreement No. 798411; Swiss National Science Foundation Ambizione Grant PZ00P2_202188; Swiss National Science Foundation PRIMA Grant No. 179834; Gordon and Betty Moore Foundation Symbiosis in Aquatic Systems Initiative Investigator Award GBMF9197; Simons Foundation Principles of Microbial Ecosystems (PriME) collaboration Grant 542395FY22; Alon scholarship (Council for Higher Education, Israel)
Funding text :
We thank Dr. Russell Naisbit for his help with editing the manuscript and members of the Simons Foundation PriME collaboration for fruitful discussions. We gratefully acknowledge funding from the European Molecular Biology Organization (EMBO; ALTF 1109-2016), from the Human Frontier Science Program (HFSP; LT001209/2017) and Alon scholarship (Council for Higher Education, Israel) to U.A.; from an ETH Postdoc Fellowship to A.N.; from the European Union’s Horizon 2020 research and innovation program under a Marie Skłodowska-Curie grant agreement (No. 798411) to F.J.P.; from a Swiss National Science Foundation Ambizione Grant (PZ00P2_202188) to J.S.; from a Swiss National Science Foundation PRIMA Grant (No. 179834) to E.S.; from the Luxembourg National Research Fund’s ATTRACT Investigator Grant (Grant no. A17/MS/11572821/MBRACE) and CORE Grant (C19/MS/13719464/TOPOFLUME/Sengupta) to A.S.; and from a Gordon and Betty Moore Foundation Symbiosis in Aquatic Systems Initiative Investigator Award (GBMF9197), and from the Simons Foundation through the Principles of Microbial Ecosystems (PriME) collaboration (grant 542395FY22) to R.S.
P.W. Boyd H. Claustre M. Levy D.A. Siegel T. Weber Multi-faceted particle pumps drive carbon sequestration in the ocean Nature 568 327 335 2019Natur.568.327B 1:CAS:528:DC%2BC1MXovFaqs7Y%3D 30996317 10.1038/s41586-019-1098-2
M.H. Iversen Carbon export in the Ocean: A biologist’s perspective Ann. Rev. Mar. Sci. 15 357 381 36055975 0657.58003 10.1146/annurev-marine-032122-035153
D.A. Siegel T. DeVries I. Cetinić K.M. Bisson Quantifying the Ocean’s biological pump and its carbon cycle impacts on global scales Ann. Rev. Mar. Sci. 15 329 356 36070554 10.1146/annurev-marine-040722-115226
K.O. Buesseler P.W. Boyd Shedding light on processes that control particle export and flux attenuation in the twilight zone of the open ocean Limnol. Oceanogr. 54 1210 1232 2009LimOc.54.1210B 1:CAS:528:DC%2BD1MXhsVCrt7%2FE 10.4319/lo.2009.54.4.1210
N. Briggs G. Dall’Olmo H. Claustre Major role of particle fragmentation in regulating biological sequestration of CO2 by the oceans Science 367 791 793 2020Sci..367.791B 1:CAS:528:DC%2BB3cXjtFehsb8%3D 32054763 10.1126/science.aay1790
F. Li et al. Planktonic microbial signatures of sinking particle export in the open ocean’s interior Nat. Commun. 14 2023NatCo.14.7177L 1:CAS:528:DC%2BB3sXitlaqsLnE 37935690 10630432 1431.94141 10.1038/s41467-023-42909-9 7177
Stephens, B. M. et al. Direct observations of microbial community succession on sinking marine particles. ISME J18, https://doi.org/10.1093/ismejo/wrad010 (2024).
D.A. Siegel et al. Prediction of the export and fate of global ocean net primary production: The exports science plan Front. Mar. Sci. 3 1 10 0075.25103 10.3389/fmars.2016.00022
J.P. Dunne J.L. Sarmiento A. Gnanadesikan A synthesis of global particle export from the surface ocean and cycling through the ocean interior and on the seafloor Glob. Biogeochem. Cycles 21 1 16 10.1029/2006GB002907
J.H. Martin G.A. Knauer D.M. Karl W.W. Broenkow VERTEX: carbon cycling in the northeast Pacific Deep Sea Res. Part A, Oceanogr. Res. Pap. 34 267 285 1987DSRA..34.267M 1:CAS:528:DyaL2sXks1Cgs7Y%3D 10.1016/0198-0149(87)90086-0
R.A. Armstrong C. Lee J.I. Hedges S. Honjo S.G. Wakeham A new, mechanistic model for organic carbon fluxes in the ocean based on the quantitative association of POC with ballast minerals Deep Sea Res. Part II: Topical Stud. Oceanogr. 49 219 236 2001DSRII.49.219A 10.1016/S0967-0645(01)00101-1
A. Alldredge The carbon, nitrogen and mass content of marine snow as a function of aggregate size Deep Sea Res. Part I: Oceanogr. Res. Pap. 45 529 541 1998DSRI..45.529A 1:CAS:528:DyaK1cXlsVOiurY%3D 1349.82067 10.1016/S0967-0637(97)00048-4
I. Klawonn et al. Fungal parasitism on diatoms alters formation and bio–physical properties of sinking aggregates Commun. Biol. 6 206 1:CAS:528:DC%2BB3sXjslemsro%3D 36810576 9944279 1020.03053 10.1038/s42003-023-04453-6
G.A. Jackson A model of the formation of marine algal flocs by physical coagulation processes Deep Sea Res. Part A. Oceanogr. Res. Pap. 37 1197 1211 1990DSRA..37.1197J 1071445 1:CAS:528:DyaK3MXhvFWqsb8%3D 1484.11119 10.1016/0198-0149(90)90038-W
A.B. Burd G.A. Jackson Particle aggregation Ann. Rev. Mar. Sci. 1 65 90 21141030 1183.62006 10.1146/annurev.marine.010908.163904
T. Nagata Y. Yamada H. Fukuda Transparent exopolymer particles in deep Oceans: Synthesis and future challenges Gels 7 75 1:CAS:528:DC%2BB3MXisVCqsrvJ 34206532 8293251 0776.05021 10.3390/gels7030075
X. Mari U. Passow C. Migon A.B. Burd L. Legendre Transparent exopolymer particles: Effects on carbon cycling in the ocean Prog. Oceanogr. 151 13 37 2017PrOce.151..13M 10.1016/j.pocean.2016.11.002
Y. Yamada H. Fukuda K. Inoue K. Kogure T. Nagata Effects of attached bacteria on organic aggregate settling velocity in seawater Aquat. Microb. Ecol. 70 261 272 10.3354/ame01658
Y. Yamada et al. Localized accumulation and a shelf-basin gradient of particles in the Chukchi Sea and Canada Basin, western Arctic J. Geophys. Res. Oceans 120 4638 4653 2015JGRC.120.4638Y 1318.28014 10.1002/2015JC010794
P. Verdugo Marine microgels Ann. Rev. Mar. Sci. 4 375 400 22457980 10.1146/annurev-marine-120709-142759
Engel, A, Endres, S, Galgani, L. & Schartau, M. Marvelous marine microgels: On the distribution and impact of gel-like particles in the Oceanic water-column. Front. Mar. Sci. 7, https://doi.org/10.3389/fmars.2020.00405 (2020).
E. Bar-Zeev I. Berman-Frank O. Girshevitz T. Berman Revised paradigm of aquatic biofilm formation facilitated by microgel transparent exopolymer particles Proc. Natl Acad. Sci. USA 109 9119 9124 2012PNAS.109.9119B 1:CAS:528:DC%2BC38XovF2gu70%3D 22615362 3384133 10.1073/pnas.1203708109
K.N. Kragh T. Tolker-Nielsen M. Lichtenberg The non-attached biofilm aggregate Commun. Biol. 6 898 37658117 10474055 07921640 10.1038/s42003-023-05281-4
H.-C. Flemming S. Wuertz Bacteria and archaea on Earth and their abundance in biofilms Nat. Rev. Microbiol. 17 247 260 1:CAS:528:DC%2BC1MXmsVylsrk%3D 30760902 10.1038/s41579-019-0158-9
A. Gärdes M.H. Iversen H.P. Grossart U. Passow M.S. Ullrich Diatom-associated bacteria are required for aggregation of Thalassiosira weissflogii ISME J. 5 436 445 20827289 10.1038/ismej.2010.145
M. Simon H.H.P. Grossart B. Schweitzer H. Ploug Microbial ecology of organic aggregates in aquatic ecosystems Aquat. Microb. Ecol. 28 175 211 10.3354/ame028175
Verdugo, P. et al. The oceanic gel phase: A bridge in the DOM-POM continuum. in Mar. Chem.92, 67–85 (2004).
C. Vernette et al. The Ocean Gene Atlas v2.0: online exploration of the biogeography and phylogeny of plankton genes Nucleic Acids Res. 50 W516 W526 1:CAS:528:DC%2BB3sXpsF2qsb0%3D 35687095 9252727 10.1093/nar/gkac420
H.P. Grossart et al. Interactions between marine snow and heterotrophic bacteria: Aggregate formation and microbial dynamics Aquat. Microb. Ecol. 42 19 26 10.3354/ame042019
H. Ploug B.B. Jørgensen A net-jet flow system for mass transfer and microsensor studies of sinking aggregates Mar. Ecol. Prog. Ser. 176 279 290 1999MEPS.176.279P 1:CAS:528:DyaK1MXhsFOhsbc%3D 1279.03009 10.3354/meps176279
Koch, H. et al. Genomic, metabolic and phenotypic variability shapes ecological differentiation and intraspecies interactions of Alteromonas macleodii. Sci. Rep.10, 809 (2020).
Robertson, J. M. et al. Marine bacteria Alteromonas spp. require UDP-glucose-4-epimerase for aggregation and production of sticky exopolymer. mBio15, e00038-24 (2024).
Y. Yawata et al. Competition-dispersal tradeoff ecologically differentiates recently speciated marine bacterioplankton populations Proc. Natl. Acad. Sci. USA 111 5622 5627 2014PNAS.111.5622Y 1:CAS:528:DC%2BC2cXltl2htrw%3D 24706766 3992678 10.1073/pnas.1318943111
Verdugo, P. et al. Marine biopolymer self-assembly: Implications for carbon cycling in the ocean. Faraday Discuss.139, 393–398 (2008).
X. Mari S. Beauvais R. Lemée M.L. Pedrotti Non‐Redfield C:N ratio of transparent exopolymeric particles in the northwestern Mediterranean Sea Limnol. Oceanogr. 46 1831 1836 2001LimOc.46.1831M 1:CAS:528:DC%2BD3MXovVGnt7c%3D 10.4319/lo.2001.46.7.1831
Devresse, Q, Becker, K. W. & Engel, A. Distribution of polysaccharidic and proteinaceous gel−like particles in three cyclonic eddies in the Eastern Tropical North Atlantic. Front. Mar. Sci. 11, https://doi.org/10.3389/fmars.2024.1357646 (2024).
M. Gralka S. Pollak O.X. Cordero Genome content predicts the carbon catabolic preferences of heterotrophic bacteria Nat. Microbiol. 8 1799 1808 1:CAS:528:DC%2BB3sXhvVaisb3O 37653010 10.1038/s41564-023-01458-z
Stokes, G. G. On the Effect of the Internal Friction of Fluids on the Motion of Pendulums. 6 (University Press, Cambridge, 1851).
Azetsu-Scott, K. & Passow, U. Ascending marine particles: Significance of transparent exopolymer particles (TEP) in the upper ocean. Limnol. Oceanogr.49, 741–748 (2004).
S.K. Friedlander Mass and heat transfer to single spheres and cylinders at low Reynolds numbers AIChE J. 3 43 48 1957AIChE..3..43F 1:CAS:528:DyaG2sXkvF2nsg%3D%3D 0628.10039 10.1002/aic.690030109
X. Mari A. Burd Seasonal size spectra of transparent exopolymeric particles (TEP) in a coastal sea and comparison with those predicted using coagulation theory Mar. Ecol. Prog. Ser. 163 63 76 1998MEPS.163..63M 1:CAS:528:DyaK1cXit1SjtbY%3D 1320.62080 10.3354/meps163063
S.M. Myklestad Release of extracellular products by phytoplankton with special emphasis on polysaccharides Sci. Total Environ. 165 155 164 1995ScTEn.165.155M 1:CAS:528:DyaK2MXlsFGrt74%3D 1422.74002 10.1016/0048-9697(95)04549-G
S. Seebah C. Fairfield M.S. Ullrich U. Passow Aggregation and sedimentation of Thalassiosira weissflogii (diatom) in a warmer and more acidified future Ocean PLoS ONE 9 2014PLoSO..9k2379S 25375640 4223051 10.1371/journal.pone.0112379 e112379
P. Tréguer et al. Influence of diatom diversity on the ocean biological carbon pump Nat. Geosci. 11 27 37 2018NatGe.11..27T 0825.76688 10.1038/s41561-017-0028-x
Romanelli, E, Sweet, J, Giering, S. L. C, Siegel, D. A. & Passow, U. The importance of transparent exopolymer particles over ballast in determining both sinking and suspension of small particles during late summer in the Northeast Pacific Ocean. Elem. Sci. Anth. 11, https://doi.org/10.1525/elementa.2022.00122 (2023).
Yamada, Y. et al. Functions of extracellular polymeric substances in partitioning suspended and sinking particles in the upper oceans of two open ocean systems. Limnol. Oceanogr.https://doi.org/10.1002/lno.12554 (2024).
R. Chajwa E. Flaum K.D. Bidle B. Van Mooy M. Prakash Hidden comet tails of marine snow impede ocean-based carbon sequestration Science 386 eadl5767 1:CAS:528:DC%2BB2cXit1ait7zK 39388567 10.1126/science.adl5767
D. Krishnamurthy et al. Scale-free vertical tracking microscopy Nat. Methods 17 1040 1051 1:CAS:528:DC%2BB3cXhs1WrurbF 32807956 1481.82034 10.1038/s41592-020-0924-7
T.T.H. Nguyen et al. Microbes contribute to setting the ocean carbon flux by altering the fate of sinking particulates Nat. Commun. 13 2022NatCo.13.1657N 1:CAS:528:DC%2BB38Xos1Ors70%3D 35351873 8964765 1304.16014 10.1038/s41467-022-29297-2 1657
U. Alcolombri et al. Sinking enhances the degradation of organic particles by marine bacteria Nat. Geosci. 14 775 780 2021NatGe.14.775A 1:CAS:528:DC%2BB3MXitFSgurjE 0077.37807 10.1038/s41561-021-00817-x
K. Avila et al. The onset of turbulence in pipe flow Science 333 192 196 2011Sci..333.192A 1:CAS:528:DC%2BC3MXotlGmtLY%3D 21737736 1411.76035 10.1126/science.1203223
F. Delplace Laminar flow of Newtonian liquids in ducts of rectangular cross-section a model for both physics and mathematics Open Access J. Math. Theor. Phys. 1 198 201 07920285 10.15406/oajmtp.2018.01.00034
Allan, D. B, Caswell, T, Keim, N. C, van der Wel, C. M. & Verweij, R. W. soft-matter/trackpy: Trackpy v0.5.0 https://doi.org/10.5281/ZENODO.4682814 (2021).
Y. Liu et al. Preparation and characterization of intracellular and exopolysaccharides during cycle cultivation of Spirulina platensis Foods 12 1067 1:CAS:528:DC%2BB3sXls1ehsLk%3D 36900580 10000700 1529.35237 10.3390/foods12051067
S.N. Aslam T. Cresswell‐Maynard D.N. Thomas G.J.C. Underwood Production and characterization of the intra‐ and extracellular carbohydrates and polymeric substances (EPS) of three sea‐ice diatom species, and evidence for a cryoprotective role for EPS J. Phycol. 48 1494 1509 1:CAS:528:DC%2BC3sXhsFegtLo%3D 27009999 10.1111/jpy.12004
M.A. Kumar K.T.K. Anandapandian K. Parthiban Production and characterization of exopolysaccharides (EPS) from biofilm forming marine bacterium Braz. Arch. Biol. Technol. 54 259 265 1:CAS:528:DC%2BC3MXoslOhtrk%3D 10.1590/S1516-89132011000200006
C. Rizzo et al. Characterization of the exopolymer-producing Pseudoalteromonas sp. S8-8 from Antarctic sediment Appl. Microbiol. Biotechnol. 106 7173 7185 1:CAS:528:DC%2BB38XisV2nsrnN 36156161 9592659 0941.35086 10.1007/s00253-022-12180-x
N. Srivastava S. Kumari S. Kurmi A.K. Pinnaka A.R. Choudhury Isolation, purification, and characterization of a novel exopolysaccharide isolated from marine bacteria Brevibacillus borstelensis M42 Arch. Microbiol 204 399 1:CAS:528:DC%2BB38XhsFCrsbvM 35713724 10.1007/s00203-022-02993-9
B. Rühmann J. Schmid V. Sieber Fast carbohydrate analysis via liquid chromatography coupled with ultra violet and electrospray ionization ion trap detection in 96-well format J. Chromatogr. A 1350 44 50 24861788 1203.37088 10.1016/j.chroma.2014.05.014
G. Xu M.J. Amicucci Z. Cheng A.G. Galermo C.B. Lebrilla Revisiting monosaccharide analysis – quantitation of a comprehensive set of monosaccharides using dynamic multiple reaction monitoring Analyst 143 200 207 2018Ana..143.200X 1:CAS:528:DC%2BC2sXhvVGmtrfJ 10.1039/C7AN01530E
