Articles | Volume 22, issue 20
https://doi.org/10.5194/bg-22-5787-2025
© Author(s) 2025. This work is distributed under
the Creative Commons Attribution 4.0 License.
the Creative Commons Attribution 4.0 License.
https://doi.org/10.5194/bg-22-5787-2025
© Author(s) 2025. This work is distributed under
the Creative Commons Attribution 4.0 License.
the Creative Commons Attribution 4.0 License.
Research article
| 
21 Oct 2025
Research article |
| 21 Oct 2025
| 21 Oct 2025
Carbohydrates, enzyme activities, and microbial communities across depth gradients in the western North Atlantic Ocean
C. Chad Lloyd
Department of Earth, Marine, and Environmental Sciences, University of North Carolina at Chapel Hill, Chapel Hill, NC, USA
Sarah Brown
Environment, Ecology, and Energy Program, University of North Carolina at Chapel Hill, Chapel Hill, NC, USA
Greta Giljan
Department of Molecular Ecology, Max Planck Institute for Marine Microbiology, Bremen, Germany
Sherif Ghobrial
Department of Earth, Marine, and Environmental Sciences, University of North Carolina at Chapel Hill, Chapel Hill, NC, USA
Silvia Vidal-Melgosa
Department of Molecular Ecology, Max Planck Institute for Marine Microbiology, Bremen, Germany
MARUM, Center for Marine Environmental Sciences, University of Bremen, Bremen, Germany
Nicola Steinke
MARUM, Center for Marine Environmental Sciences, University of Bremen, Bremen, Germany
Jan-Hendrik Hehemann
Department of Molecular Ecology, Max Planck Institute for Marine Microbiology, Bremen, Germany
MARUM, Center for Marine Environmental Sciences, University of Bremen, Bremen, Germany
Rudolf Amann
Department of Molecular Ecology, Max Planck Institute for Marine Microbiology, Bremen, Germany
Carol Arnosti
CORRESPONDING AUTHOR
Department of Molecular Ecology, Max Planck Institute for Marine Microbiology, Bremen, Germany
Department of Earth, Marine, and Environmental Sciences, University of North Carolina at Chapel Hill, Chapel Hill, NC, USA
Related authors
C. Chad Lloyd, Sarah Brown, Greta Giljan, Sherif Ghobrial, Silvia Vidal-Melgosa, Nicola Steinke, Jan-Hendrik Hehemann, Rudolf Amann, and Carol Arnosti
EGUsphere, https://doi.org/10.5194/egusphere-2024-615, https://doi.org/10.5194/egusphere-2024-615, 2024
Preprint archived
Short summary
Short summary
The cycling of carbon throughout the ocean is dependent on the balance between phytoplankton productivity and heterotrophic decomposition. Bacteria must produce structurally specific enzymes to degrade specific chemical structures found in organic matter. We found distinct correlations between the organic matter composition, bacterial community structure, and potential enzymatic activities with depth, and found that the structural complexity of organic matter varies with location in the ocean.
C. Chad Lloyd, Sarah Brown, Greta Giljan, Sherif Ghobrial, Silvia Vidal-Melgosa, Nicola Steinke, Jan-Hendrik Hehemann, Rudolf Amann, and Carol Arnosti
EGUsphere, https://doi.org/10.5194/egusphere-2024-615, https://doi.org/10.5194/egusphere-2024-615, 2024
Preprint archived
Short summary
Short summary
The cycling of carbon throughout the ocean is dependent on the balance between phytoplankton productivity and heterotrophic decomposition. Bacteria must produce structurally specific enzymes to degrade specific chemical structures found in organic matter. We found distinct correlations between the organic matter composition, bacterial community structure, and potential enzymatic activities with depth, and found that the structural complexity of organic matter varies with location in the ocean.
Sarah A. Brown, John Paul Balmonte, Adrienne Hoarfrost, Sherif Ghobrial, and Carol Arnosti
Biogeosciences, 19, 5617–5631, https://doi.org/10.5194/bg-19-5617-2022, https://doi.org/10.5194/bg-19-5617-2022, 2022
Short summary
Short summary
Bacteria use extracellular enzymes to cut large organic matter to sizes small enough for uptake. We compared the enzymatic response of surface, mid-water, and deep-ocean bacteria to complex natural substrates. Bacteria in surface and mid-depth waters produced a much wider range of enzymes than those in the deep ocean and may therefore consume a broader range of organic matter. The extent to which organic matter is recycled by bacteria depends in part on its residence time at different depths.
Cited articles
Alderkamp, A.-C., Van Rijssel, M., and Bolhuis, H.: Characterization of marine bacteria and the activity of their enzyme systems involved in degradation of the algal storage glucan laminarin, FEMS Microbiol. Ecol., 59, 108–117, 2007.
Andres, M., Muglia, M., Bahr, F., and Bane, J.: Continuous flow of Upper Labrador Sea Water around Cape Hatteras, Sci. Rep., 8, 4494, https://doi.org/10.1038/s41598-018-22758-z, 2018.
Arnosti, C.: Fluorescent derivatization of polysaccharides and carbohydrate-containing biopolymers for measurement of enzyme activities in complex media, J. Chromatogr. B. Analyt. Technol. Biomed. Life Sci., 793, 181–191, https://doi.org/10.1016/s1570-0232(03)00375-1, 2003.
Arnosti, C.: Microbial extracellular enzymes and the marine carbon cycle, Ann. Rev. Mar. Sci., 3, 401–425, https://doi.org/10.1146/annurev-marine-120709-14273, 2011.
Arnosti, C.: Large substrate hydrolysis of bulk water samples taken aboard the R/V Endeavor EN638, May 2019 in the Northern Atlantic. (Version 1), Biological and Chemical Oceanography Data Management Office (BCO-DMO) [data set], https://doi.org/10.26008/1912/BCO-DMO.821801.1, 2020a.
Arnosti, C.: Small substrate hydrolysis of bulk water samples taken aboard the R/V Endeavor EN638, May 2019 in the Northern Atlantic. (Version 1), Biological and Chemical Oceanography Data Management Office (BCO-DMO) [data set], https://doi.org/10.26008/1912/BCO-DMO.820973.1, 2020b.
Arnosti, C.: Bulk water cell abundance of samples taken aboard the R/V Endeavor EN638, May 2019 in the Northern Atlantic (Version 1), Biological and Chemical Oceanography Data Management Office (BCO-DMO) [data set], https://doi.org/10.26008/1912/BCO-DMO.820961.1, 2020c.
Arnosti, C.: Bacterial production of bulk water and large volume samples taken aboard the R/V Endeavor EN638, May 2019 in the Northern Atlantic. (Version 1), Biological and Chemical Oceanography Data Management Office (BCO-DMO) [data set], https://doi.org/10.26008/1912/BCO-DMO.820556.1, 2020d.
Arnosti, C., Steen, A. D., Ziervogel, K., Ghobrial, S., and Jeffrey, W. H.: Latitudinal gradients in degradation of marine dissolved organic carbon, PLoS ONE, 6, e28900, https://doi.org/10.1371/journal.pone.0028900, 2011.
Arnosti, C., Fuchs, B., Amann, R., and Passow, U.: Contrasting extracellular enzyme activities of particle associated bacteria from distinct provinces of the North Atlantic Ocean, Front. Microbiol., 3, 425, https://doi.org/10.3389/fmicb.2012.00425, 2012.
Arnosti, C., Wietz, M., Brinkhoff, T., Hehemann, J.-H., Probandt, D., Zeugner, L., and Amann, R.: The biogeochemistry of marine polysaccharides: Sources, inventories, and bacterial drivers of the carbohydrate cycle, Annu. Rev. Mar. Sci., 13, https://doi.org/10.1146/annurev-marine-032020-012810, 2021.
Arnosti, C., Hoarfrost, A., Balmonte, J. P., Lloyd, C. C., Brown, S. A., and Ghobrial, S.: Empirical definition of the mad buckets magic number: A guide for seagoing scientists, L&O Bull., 32, 104, https://doi.org/10.1002/lob.10577, 2023.
Avci, B., Kruger, K., Fuchs, B. M., Teeling, H., and Amann, R. I.: Polysaccharide niche partitioning of distinct Polaribacter clades during North Sea spring algal blooms, ISME J., 14, 1369–1383, 2020.
Azam, F., and Malfatti, F.: Microbial structuring of marine ecosystems, Nat. Rev. Microbiol., 5, 782–791, https://doi.org/10.1038/nrmicro1747, 2007.
Baker, C. A., Henson, S. A., Cavan, E. L., Giering, S. L. C., Yool, A., Gehlen, M., Belcher, A., Riley, J. S., Smith, H. E. K., and Sanders, R.: Slow-sinking particulate organic carbon in the Atlantic Ocean: Magnitude, flux, and potential controls, Global Biogeochem. Cy., 31, 105101065, https://doi.org/10.1002/2017GB005638, 2017.
Balmonte, J. P., Teske, A., and Arnosti, C.: Structure and function of high Arctic pelagic, particle-associated and benthic bacterial communities, Environ. Microbiol., 20, 2941–2959, 2018.
Balmonte, J. P., Simon, M., Giebel, H.-A., and Arnosti, C.: A sea change in microbial enzymes: Heterogeneous latitudinal and depth-related gradients in bulk water and particle-associated enzymatic activities from 30° S to 59° N in the Pacific Ocean, Limnol. Ocean., 66, 3489–3507, https://doi.org/10.1002/lno.11894, 2021.
Becker, S., Tebben, J., Coffinet, S., Hehemann, J.-H.: Laminarin is a major molecule in the marine carbon cycle, P. Natl. Acad. Sci. USA, 117, 6599–6607, https://doi.org/10.1073/pnas.1917001117, 2020.
Bennke, C. M., Reintjes, G., Schattenhofer, M., Ellrott, A., Wulf, J., Zeder, M., and Fuchs, B. M.: Modification of a high-throughput automatic microbial cell enumeration system for shipboard analyses, Appl. Environ. Microbiol., 82, 3289–3296, 2016.
Bligh, M., Nguyen, N., Buck-Wiese, H., Vidal-Melgosa, S., Hehemann, J.-H.: Structures and functions of algal glycans shape their capacity to sequester carbon in the ocean, Curr. Opin. Chem. Biol., 71, 102204, https://doi.org/10.1016/j.cbpa.2022.102204, 2022.
Bolaños, L., Karp-Boss, L., Choi, C., Worden, A., Graff, J., Haentjens, N., Chase, A., Penna, A., Gaube, P., Morison, F., Menden-Deuer, S., Westberry, T., O'Malley, R., Boss, E., Behrenfeld, M., and Giovannoni, S.: Small phytoplankton dominate western North Atlantic biomass, ISME J., 14, 1663–1674, https://doi.org/10.1038/s41396-020-0636-0, 2020.
Boyd, P. W., Sherry, N. D., Berges, J. A., Bishop, J. K. B., Calvert, S. E., Charette, M. A., Giovannoni, S. J., Goldblatt, R., Harrison, P. J., Moran, S. B., Roy, S., Soon, M., Strom, S., Thibault, D., Vergin, K. L., Whitney, F. A., and Wong, C. S.: Transformations of biogenic particulates from the pelagic to the deep ocean realm, Deep-Sea Res. Pt. II, 46, 2761–2792, 1999.
Broecker, W.: The great ocean conveyor, Oceanography, 4, 79–89, https://doi.org/10.5670/oceanog.1991.07, 1991.
Buck-Wiese, H., Andskog, M. A., Nguyen, N. P., Asmala, E., Vidal-Melgosa, S., Liebke, M., Gustafsson, C., and Hehemann, J.-H.: Fucoid brown algae inject fucoidan carbon into the ocean, P. Natl. Acad. Sci. USA, 120, e2210561119, https://doi.org/10.1073/pnas.2210561119, 2023.
Buesseler, K. O., Lamborg, C. H., Boyd, P. W., Lam, P. J., Trull, T. W., Bidigare, R. R., Bishop, J. K., Casciotti, K. L., Dehairs, F., Elskens, M., Honda, M., Karl, D. M., Siegel, D. A., Silver, M. W., Steinberg, D. K., Valdes, J., Van Mooy, B., and Wilson, S.: Revisiting carbon flux through the ocean's twilight zone, Science, 316, 567–570, 2007.
Bushnell, B.: BBTools software package, 578, http://sourceforge.net/projects/bbmap (last access: November 2023), 2014.
Cuskin, F., Lowe, E. C., Temple, M. J., Zhu, Y., Cameron, E. A., Pudlo, N. A., Porter, N. T., Urs, K., Thompson, A. J., Cartmell, A., Rogowski, A., Hamilton, B. S., Chen, R., Tolbert, T. J., Piens, K., Bracke, D., Vervecken, W., Hakki, Z., Speciale, G., Munoz-Munoz, J. L., Day, A., Pena, M. J., McLean, R., Suits, M. D., Boraston, A. B., Atherly, T., Ziemer, C. J., Williams, S. J., Davies, G. J., Abbott, D. W., Martens, E. C., and Gilbert, H. J.: Human gut Bacteroidetes can utilize yeast mannan through a selfish mechanism, Nature, 517, 165–169, 2015.
Della Penna, A. and Gaube, P.: Overview of (Sub)mesoscale ocean dynamics for the NAAMES field program, Frontiers Mar. Sci., 6, 384, https://doi.org/10.3389/fmars.2019.00384, 2019.
DeLong, E. F., Preston, C. M., Mincer, T., Rich, V., Hallam, S. J., Frigaard, N.-U., Martinez, A., Sullivan, M. B., Edwards, R., Brito, B. R., Chisholm, S. W., and Karl, D. M.: Community genomics among stratified microbial assemblages in the ocean's interior, Science, 311, 496–503, 2006.
Dlugosch, L., Bunse, C., Bunk, B., Böttcher, L., Tran, D. Q., Dittmar, T., Hartmann, M., Heinrichs, M., Hintz, N. H., Milke, F., Mori, C., Niggemann, J., Spröer, C., Striebel, M., and Simon, M.: Naturally induced biphasic phytoplankton spring bloom reveals rapid and distinct substrate and bacterial community dynamics, FEMS Microbiol. Ecol., 99, fiad078, https://doi.org/10.1093/femsec/fiad078, 2023.
Engel, A. and Handel, B.: A novel protocol for determining the concentration and composition of sugars in particulate and in high molecular weight dissolved organic matter (HMW-DOM) in seawater, Mar. Chem., 127, 180–191, https://doi.org/10.1016/j.marchem.2011.09.004, 2011.
Fadeev, E., Cardozo-Mino, M. G., Rapp, J. Z., Bienhold, C., Salter, I., Salman-Carvalho, V., Molari, M., Tegetmeyer, H. E., Buttigieg, P. L., and Boetius, A.: Comparison of two 16S rRNA primers (V3-V4 and V4-V-5) for studies of Arctic microbial communities, Frontiers Microb., 12, 637526, https://doi.org/10.3389/fmicb.2021.637526, 2021.
Follett, C. L., Repeta, D. J., Rothman, D. H., Xu, L., and Santinelli, C.: Hidden cycle of dissolved organic carbon in the deep ocean, P. Natl. Acad. Sci. USA, 111, 16706–16711, 2014.
Francis, B. T., Bartosik, D., Sura, T., Sichert, A., Hehemann, J.-H., Markert, S., Schweder, T., Fuchs, B. M., Teeling, H., Amann, R. I., and Becher, D.: Changing expression of TonB-dependent transporters suggest shifts in polysaccharide consumption over the course of a spring phytoplankton bloom, ISME J., 15, 2336–2350, https://doi.org/10.1038/s41396-021-00928-8, 2021.
Fratantoni, P. S. and Pickart, R. S.: The western North Atlantic shelfbreak current system in summer, J. Phys. Oceanogr, 37, 2509–2533, 2007.
Giljan, G., Brown, S., Lloyd, C. C., Ghobrial, S., Amann, R., and Arnosti, C.: Selfish bacteria are active throughout the water column of the ocean, ISME Commun., 3, 11, https://doi.org/10.1038/s43705-023-00219-7, 2023.
Gügi, B., Le Cosaouec, T., Burel, C., Lerouge, P., Helbert, W., and Bardor, M.: Diatom-specific oligosaccharide and polysaccharide structures help to unravel biosynthetic capabilities in diatoms, Mar. Drugs, 13, 5993–6018, 2015.
Handa, N. and Tominaga, H.: A detailed analysis of carbohydrates in marine particulate matter Mar. Biol., 2, 228–235, 1969.
Handa, N. and Yanagi, K.: Studies on water-extractable carbohydrates of the particulate matter from the northwest Pacific Ocean, Mar. Biol., 4, 197–207, 1969.
Hedges, J. I., Baldock, J. A., Gelinas, Y., Lee, C., Peterson, M., and Wakeham, S. G.: Evidence for non-selective preservation of organic matter in sinking marine particles, Nature, 409, 801–804, 2001.
Hedges, J. I., Baldock, J. A., Gelinas, Y., Lee, C., Peterson, M., and Wakeham, S. G.: The biochemical and elemental compositions of marine plankton: a NMR perspective, Mar. Chem., 78, 47–63, 2002.
Hedges, J. I., Eglinton, G., Hatcher, P. G., Kirchman, D. L., Arnosti, C., Derenne, S., Evershed, R. P., Kögel-Knabner, I., De Leeuw, J. W., Littke, R., Michaelis, W., and Rullkötter, J.: The molecularly-uncharacterized component (MUC) of nonliving organic matter in natural environments, Organic Geochem., 31, 945–958, 2000.
Heidrich, J. and Todd, R. E.: Along-stream evolution of Gulf Stream volume transport, J. Phys. Oceanogr., 50, 2251–2270, https://doi.org/10.1175/JPO-D-19-0303.1, 2020.
Herlemann, D. P. R., Labrenz, M., Jürgens, K., Bertilsson, S., Waniek, J. J., and Andersson, A. F.: Transitions in bacterial communities along the 2000 km salinity gradient of the Baltic Sea, ISME J., 5, 1571–1579, 2011.
Hoarfrost, A. and Arnosti, C.: Heterotrophic extracellular enzymatic activities in the Atlantic Ocean follow patterns across spatial and depth regimes, Front. Mar. Sci., 4, 200, https://doi.org/10.3389/fmars.2017.00200, 2017.
Huang, G., Vidal-Melgosa, S., Sichert, A., Becker, S., Fang, Y., Niggemann, J., Iversen, M. H., Cao, Y., and Hehemann, J.-H.: Secretion of sulfated fucans by diatoms may contribute to marine aggregate formation, Limnol. Oceanography, 66, 3768–3782, 2021.
Iversen, M. H.: Carbon export in the ocean: A biologist's perspective, Annu. Rev. Mar. Sci., 15, 357–381, 2023.
Kalenborn, S., Zuhlke, D., Riedel, K., Amann, R. I., and Harder, J.: Proteomic insight into arabinogalactan utilization by particle-associated Maribacter sp. MAR_2009_72, FEMS Microb. Ecol., 100, fiae045, https://doi.org/10.1093/femsec/fiae045, 2024.
Kharbush, J., Close, H., Van Mooy, B., Arnosti, C., Smittenberg, R., Le Moigne, F., Molienhauer, G., Scholz-Bottcher, B., Obreht, I., Koch, B., Becker, K., Iversen, M., and Mohr, W.: Particulate organic carbon Deconstructed: Molecular and chemical composition of particulate organic carbon in the ocean, Front. Mar. Sci., 7, 00518, https://doi.org/10.3389/fmars.2020.00518, 2020.
Kirchman, D. L.: Measuring bacterial biomass production and growth rates from leucine incorporation in natural aquatic environments, Methods Microbiol., 30, 227–237, https://doi.org/10.1016/s0580-9517(01)30047-8, 2001.
Koch, H., Dürwald, A., Schweder, T., Noriega-Ortega, B., Vidal-Melgosa, S., Hehemann, J.-H., Dittmar, T., Freese, H. M., Becher D., Simon, M., and Wietz, M.: Biphasic cellular adaptations and ecological impllications of Alteromonas macleodii degrading a mixture of algal polysaccharides, ISME J., 13, 92–103, https://doi.org/10.1038/s41396-018-0252-4, 2019.
Krüger, K., Chafee, M., Francis, T. B., Glavina del Rio, T., Becher, D., Schweder, T., Amann, R. I., and Teeling, H.: In marine Bacteroidetes the bulk of glycan degradation during algae blooms is mediated by few clades using a restricted set of genes, ISME J., 13, 2800–2816, 2019.
Laine, R. A.: A calculation of all possible oligosaccharide isomers both branched and linear yields 1.05 x 1012 structures for a reducing hexasaccharide: the Isomer Barrier to development of single-method saccharide sequencing or synthesis systems, Glycobiology, 4, 759–767, https://doi.org/10.1093/glycob/4.6.759, 1994.
Lapébie, P., Lombard, V., Drula, E., Terrapon, N., and Henrissat, B.: Bacteroidetes use thousands of enzyme combinations to break down glycans, Nat. Commun., 10, 2043, https://doi.org/10.1038/s41467-019-10068-5, 2019.
Liu, M. and Tanhua, T.: Water masses in the Atlantic Ocean: characteristics and distributions, Ocean Sci., 17, 463–486, https://doi.org/10.5194/os-17-463-2021, 2021.
Lloyd, C. C.: Monosaccharide composition of POM-derived carbohydrates in the western North Atlantic Ocean, Zenodo [data set], https://doi.org/10.5281/zenodo.15375159, 2025a.
Lloyd, C. C.: Carbohydrate epitope analysis (via antibody probing) of POM-derived organic matter in the western North Atlantic Ocean, Zenodo [data set], https://doi.org/10.5281/zenodo.15375738, 2025b.
Lloyd, C. C., Brown, S., Balmonte, J. P., Hoarfrost, A., Ghobrial, S., and Arnosti, C.: Particles act as “specialty centers” with expanded enzymatic function throughout the water column in the western North Atlantic, Front. Microbiol., 13, 882333, https://doi.org/10.3389/fmicb.2022.882333, 2022.
Lloyd, C. C., Brown, S., Balmonte, J. P., Hoarfrost, A., Ghobrial, S., and Arnosti, C.: Links between regional and depth patterns of microbial communities and enzyme activities in the western North Atlantic Ocean, Mar. Chem., 255, 104299, https://doi.org/10.1016/j.marchem.2023.104299, 2023.
Lombard, V., Ramulu, H. G., Drula, E., Coutinho, P. M., and Henrissat, B.: The carbohydrate-active enzymes database (CAZy) in 2013, Nucleic Acids Res., 42, D490–495, https://doi.org/10.1093/mar/gkt1178, 2014.
Markussen, T. N., Konrad, C., Waldmann, C., Becker, M., Fischer, G., and Iversen, M. H.: Tracks in the snow – advantage of combining optical methods to characterize marine particles and aggregates, Front. Marine Sci., 7, 476, https://doi.org/10.3389/fmars.2020.00476, 2020.
McCarthy, M., Hedges, J., and Benner, R.: Major biochemical composition of dissolved high molecular weight organic matter in seawater, Mar. Chem., 55, 281–297, 1996.
Mestre, M., Ruiz-González, C., Logares, R., Duarte, C. M., Gasol, J. M., and Sala, M. M.: Sinking particles promote vertical connectivity in the ocean microbiome, P. Natl. Acad. Sci. USA, 115, E6799–E6807, https://doi.org/10.1073/pnas.1802470115, 2018.
Middelboe, M.: Microbial disease in the sea: effects of viruses on carbon and nutrient cycling, Princeton University Press, 242–251, ISBN 9780691124858, 2008.
Mitulla, M., Dinasquet, J., Guillemette, R., Simon, M., Azam, F., and Wietz, M.: Response of bacterial communities from California coastal waters to alginate particles and an alginolytic Alteromonas macleodii strain, Environ. Microb. 18, 4369–4377, 2016.
Morris, R. M., Nunn, B. L., Frazar, C., Goodlett, D. R., Ting, Y. S., and Rocap, G.: Comparative metaproteomics reveals ocean-scale shifts in microbial nutrient utilization and energy transduction, ISME J., 5, 673–685, 2010.
Murray, A. E., Arnosti, C., De La Rocha, C. L., Grossart, H.-P., and Passow, U.: Microbial dynamics in autotrophic and heterotrophic seawater mesocosms. II. Bacterioplankton community structure and hydrolytic enzyme activities, Aquatic Microbial Ecology, 49, 123–141, 2007.
Nagata, T. and Kirchman, D. L.: Release of dissolved organic matter by heterotrophic protozoa: implications for microbial food webs, Arch. Hydrobiol. Beij. Ergebn. Limnol., 35, 99–109, 1992.
Orellana, L. H., Francis, T. B., Ferraro, M., Hehemann, J.-H., Fuchs, B. M., and Amann, R. I.: Verrucomicrobiota are specialist consumers of sulphated methyl pentoses during diatom blooms, ISME J., 16, 630–641, 2022.
Pelve, E., Fontanez, K., and DeLong, E.: Bacterial succession on sinking particles in the ocean's interior, Front. Microbiol., 8, 2269, https://doi.org/10.3389/fmicb.2017.02269, 2017.
Poff, D. E., Leu, A. O., Eppley, J. M., Karl, D. M., and DeLong, E. F.: Microbial dynamics of elevated carbon flux in the open ocean's abyss, P. Natl. Acad. Sci. USA, 118, e2018269118, https://doi.org/10.1073/pnas.2018269118, 2021.
Priest, T., Vidal-Melgosa, S., Hehemann, J.-H., Aman, R., and Fuchs, B. M.: Carbohydrates and carbohydrate degradation gene abundance and transcription in Atlantic waters of the Arctic, ISME Comm., 3, 130, https://doi.org/10.1038/s43705-023-00324-7, 2023.
Quast, C., Pruesse, E., Yilmaz, P., Gerken, J., Schweer, T., Yarza, P., Peplies, J., and Glöckner, F. O.: The SILVA ribosomal RNA gene database project: improved data processing and web-based tools, Nuc. Acids Res., 41, 590–596, 2013.
Reintjes, G., Arnosti, C., Fuchs, B. M., and Amann, R.: An alternative polysaccharide uptake mechanism of marine bacteria, ISME J., 11, 1640–1650, https://doi.org/10.1038/ismej.2017.26, 2017.
Reisky, L., Prechoux, A., Zuhlke, M.-K., Baumgen, M., Robb, C. S., Gerlach, N., Roret, T., Stanetty, C., Larocque, R., Michel, G., Song, T., Markert, S., Unfried, F., Mihovilovic, M. D., Trautwein-Schult, A., Becher, D., Schweder, T., Bornscheuer, U. T., and Hehemann, J.-H.: A marine bacterial enzymatic cascade degrades the algal polysaccharide ulvan, Nat. Chem. Biol., 15, 803–812, 2019.
Ruiz-González, C., Mestre, M., Estrada, M., Sebastián, M., Salazar, G., Agustí, S., Moreno-Ostos, E., Reche, I., Álvarez-Salgado, X. A., Morán, X. A. G., Duarte, C. M., Sala, M. M., and Gasol, J. M.: Major imprint of surface plankton on deep ocean prokaryotic structure and activity, Mol. Ecol., 29, 1820–1838, https://doi.org/10.1111/mec.15454, 2020.
Saito, M. A., Bertrand, E. M., Duffy, M. E., Gaylord, D. A., Held, N. A., Hervey IV, W. J., Hettich, R. L., Jagtap, P. D., Janech, M. G., Kinkade, D. B., Leary, D. H., McIlvin, M. R., Moore, E. K., Morris, R. M., Neely, B. A., Nunn, B. L., Saunders, J. K., Shepherd, A. I., Symmonds, N. I., and Walsh, D. A.: Progress and challenges in ocean metaproteomics and proposed best practices for data sharing, Journal of Proteome Research, 18, 1461–1476, 2019.
Saunders, J. K., McIIvin, M. R., Dupont, C. L., Kaul, D., Moran, D. M., Horner, T., Laperriere, S. M., Webb, E. A., Bosak, T., Santoro, A. E., and Saito, M. A.: Microbial functional diversity across biogeochemical provinces in the central Pacific Ocean, P. Natl. Acad. Sci. USA 119, e2200014119, https://doi.org/10.1073/pnas.2200014119, 2022.
Sichert, A., Corzett, C. H., Schechter, M. S., Unfried, F., Markert, S., Becher, D., Fernandez-Guerra, A., Liebeke, M., Schweder, T., Polz, M. F., and Hehemann, J.-H.: Verrucomicrobia use hundreds of enzymes to digest the algal polysaccharide fucoidan, Nat. Commun., 5, 1026–1039, 2020.
Steen, A. D., Ziervogel, K., Ghobrial, S., and Arnosti, C.: Functional variation among polysaccharide-hydrolyzing microbial communities in the Gulf of Mexico, Mar. Chem., 138–139, 13–20, https://doi.org/10.1016/j.marchem/2012.06.001, 2012.
Steen, A. D., Vazin, J. P., Hagen, S. M., Mulligan, K. H., and Wilhelm, S. W.: Substrate specificity of aquatic extracellular peptidases assessed by competitive inhibition assays using synthetic substrates, Aquat. Microb. Ecol., 75, 271–281, https://doi.org/10.3354/ame01175, 2015.
Suttle, C. A.: Viruses in the sea, Nature, 437, 356–361, https://doi.org/10.1038/nature04160, 2005.
Teeling, H., Fuchs, B. M., Becher, D., Klockow, C., Gardebrecht, A., Bennke, C. M., Kassagby, M., Huang, S., Mann, A. J., Waldmann, J., Weber, M., Klindworth, A., Otto, A., Lange, J., Bernhardt, J., Reinsch, C., Hecker, M., Peplies, J., Bockelmann, F. D., Callies, U., Gerdts, G., Wichels, A., Wiltshire, K. H., Glöckner, F. O., Schweder, T., and Amann, R.: Substrate-controlled succession of marine bacterioplankton populations induced by a phytoplankton bloom, Science, 336, 608–611, 2012.
Teeling, H., Fuchs, B. M., Bennke, C. M., Krüger, K., Chafee, M., Kappelmann, L., Reintjes, G., Waldmann, J., Quast, C., Glöckner, F. O., Lucas, J., Wichels, A., Gerdts, G., Wiltshire, K. H., and Amann, R. I.: Recurring patterns in bacterioplankton dynamics during coastal spring algae blooms, eLife, 5, e11888, https://doi.org/10.7554/eLife.11888.001, 2016.
Teske, A., Durbin, A., Ziervogel, K., Cox, C., and Arnosti, C.: Microbial community composition and function in permanently cold seawater and sediments from an Arctic fjord of Svalbard, Appl. Environ. Micro., 77, https://doi.org/10.1128/AEM.01507-10, 2011.
Thomas, F., Bordron, P., Eveillard, D., and Michel, G.: Gene expression analysis of Zobellia galactanivorans during the degradation of algal polysaccharides reveals both substrate-specific and shared transcriptome-wide responses, Front. Microbiol., 81, 7385–7393, 2017.
Torode, T. A., Siméon, A., Marcus, S. E., Jam, M., Le Moigne, M.-A., Duffieux, D., Knox, J. P., and Hervé, C.: Dynamics of cell wall assembly during early embryogenesis in the brown alga Fucus, J. Exp. Bot., 67, 6089–6100, 2016.
Verdugo, P., Alldredge, A. L., Azam, F., Kirchman, D. L., Passow, U., and Santschi, P. H.: The oceanic gel phase: a bridge in the DOM-POM continuum, Mar. Chem., 92, 67–85, 2004.
Vidal-Melgosa, S., Sichert, A., Francis, T., Bartosik, D., Niggemann, J., Wichels, A., Willats, W., Fuchs, B., Teeling, H., Becher, D., Schweder, T., Amann, R., and Hehemann, J.-H.: Diatom fucan polysaccharide precipitates carbon during algal blooms, Nat. Commun., 12, 1150, https://doi.org/10.1038/s41467-021-21009-6, 2021.
Vidal-Melgosa, S., Lagator, M., Sichert, A., Priest, T., Patzold, J., and Hehemann, J.-H.: Not digested: algal glycans move carbon dioxide into the deep-sea, bioRxiv [preprint], https://doi.org/10.1101/2022.03.04.483023, 2022.
Wakeham, S. G., Lee, C., Hedges, J. I., Hernes, P. J., and Peterson, M. L.: Molecular indicators of diagenetic status in marine organic matter, Geochim. Cosmochim. Acta, 61, 5363–5369, https://doi.org/10.1016/S0016-7037(97)00312-8, 1997.
Zhao, Z., Baltar, F., and Herndl, G. J.: Linking extracellular enzymes to phylogeny indicates a predominantly particle-associated lifestyle of deep-sea prokaryotes, Sci. Adv., 6, eaaz4354, https://doi.org/10.1126/sciadv.aaz4354, 2020.
Zhou, J., Mopper, K., and Passow, U.: The role of surface-active carbohydrates in the formation of transparent exopolymer particles by bubble adsorption of seawater, Limnol. Oceanogr., 43, 1860–1871, 1998.
Zorz, J., Willis, C., Comeau, A. M., Langille, M. G. I., Johnson, C. L., Li, W. K. W., and LaRoche, J.: Drivers of regional bacterial community structure and diversity in the Northwest Atlantic Ocean, Front Microbiol., 10, 00281, https://doi.org/10.3389/fmicb.2019.00281, 2019.
Short summary
Carbon cycling throughout the ocean is dependent on the balance between phytoplankton productivity and heterotrophic decomposition. Bacteria must produce structurally specific enzymes to degrade specific chemical structures found in organic matter. Organic matter composition, environmental physical/chemical parameters, microbial community composition, and enzymatic activities varied with depth; the structural complexity of organic matter varied also with location in the ocean.
Carbon cycling throughout the ocean is dependent on the balance between phytoplankton...
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