Articles | Volume 19, issue 24
https://doi.org/10.5194/bg-19-5617-2022
© Author(s) 2022. 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-19-5617-2022
© Author(s) 2022. This work is distributed under
the Creative Commons Attribution 4.0 License.
the Creative Commons Attribution 4.0 License.
Depth-related patterns in microbial community responses to complex organic matter in the western North Atlantic Ocean
Environment, Ecology and Energy Program, University of North
Carolina at Chapel Hill, Chapel Hill, North Carolina, 27599, USA
John Paul Balmonte
Department of Earth, Marine and Environmental Sciences, University
of North Carolina at Chapel Hill, Chapel Hill, North Carolina, 27599, USA
current address: HADAL and Nordcee, Department of Biology,
University of Southern Denmark, Campusvej 55, 5230, Denmark
Adrienne Hoarfrost
Department of Earth, Marine and Environmental Sciences, University
of North Carolina at Chapel Hill, Chapel Hill, North Carolina, 27599, USA
current address: Department of Marine Sciences, University of Georgia,
Athens, Georgia, 30602, USA
Sherif Ghobrial
Department of Earth, Marine and Environmental Sciences, University
of North Carolina at Chapel Hill, Chapel Hill, North Carolina, 27599, USA
Carol Arnosti
Department of Earth, Marine and Environmental Sciences, University
of North Carolina at Chapel Hill, Chapel Hill, North Carolina, 27599, 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-2025-2249, https://doi.org/10.5194/egusphere-2025-2249, 2025
Short summary
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. We found distinct correlations between the organic matter composition, environmental physical/chemical parameters, and 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.
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, https://doi.org/10.1111/j.1574-6941.2006.00219.x, 2007.
Alonso-Sáez, L., Sánchez, O., and Gasol, J. M.: Bacterial uptake of
low molecular weight organics in the subtropical Atlantic: Are major
phylogenetic groups functionally different?, Limnol. Oceanogr., 57,
798–808, https://doi.org/10.4319/lo.2012.57.3.0798, 2012.
Amon, R. M., Fitznar, H. P., and Benner, R.: Linkages among the
bioreactivity, chemical composition, and diagenetic state of marine
dissolved organic matter, Limnol. Oceanogr., 46, 287–297,
https://doi.org/10.4319/lo.2001.46.2.0287, 2001.
Araki, T., Hashikawa, S., and Morishita, T.: Cloning, sequencing, and
expression in Escherichia coli of the new gene encoding b-1,3-xylanase from a marine
bacterium, Vibrio sp. Strain XY-214, Appl. Environ. Microb., 66, 1741–1743, 2000.
Arnosti, C.: Fluorescent derivatization of polysaccharides and
carbohydrate-containing biopolymers for measurement of enzyme activities in
complex media, J. Chromatogr. B., 793, 181–191,
https://doi.org/10.1016/S1570-0232(03)00375-1, 2003.
Arnosti, C.: Microbial extracellular enzymes and the marine carbon cycle,
Annu. Rev. Mar. Sci., 3, 401–425, https://doi.org/10.1146/annurev-marine-120709-142731,
2011.
Arnosti, C.: Project: Latitudinal and depth-related contrasts in enzymatic capabilities of pelagic microbial communities: Predictable patterns in the ocean?, BCO-DMO [data set], https://doi.org/10.26008/1912/bco-dmo.717495.1, 2018.
Arnosti, C. and Repeta, D. J.: Extracellular enzyme activity in
anaerobic bacterial cultures: Evidence of pullulanase activity among
mesophilic marine bacteria, Appl. Environ. Microb., 60, 840–846, 1994.
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.
Avcı, B., Krüger, 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, 1–15, https://doi.org/10.1038/s41396-020-0601-y,
2020.
Azam, F.: Microbial control of oceanic carbon flux: the plot
thickens, Science, 280, 694–696, https://doi.org/10.1126/science.280.5364.694, 1998.
Balmonte, J. P., Teske, A., and Arnosti, C.: Structure and function of high
Arctic pelagic, particle-associated and benthic bacterial communities,
Environ. Microbiol., 20, 2941–2954, https://doi.org/10.1111/1462-2920.14304, 2018.
Balmonte, J. P., Buckley, A., Hoarfrost, A., Ghobrial, S., Ziervogel, K.,
Teske, A., and Arnosti, C.: Community structural differences shape
microbial responses to high molecular weight organic matter, Environ.
Microbiol., 21, 557–571, https://doi.org/10.1111/1462-2920.14485, 2019.
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. Oceanogr., 66,
3489–3507, https://doi.org/10.1002/lno.11894, 2021.
Baltar, F., Arístegui, J., Sintes, E., Van Aken, H. M., Gasol, J. M.,
and Herndl, G. J.: Prokaryotic extracellular enzymatic activity in relation
to biomass production and respiration in the meso-and bathypelagic waters of
the (sub) tropical Atlantic, Environ. Microbiol., 11, 1998–2014,
https://doi.org/10.1111/j.1462-2920.2009.01922.x, 2009.
Baltar, F., Arístegui, J., Gasol, J. M., Sintes, E., van Aken, H. M.,
and Herndl, G. J.: High dissolved extracellular enzymatic activity in the
deep central Atlantic Ocean, Aquat. Microb. Ecol., 58, 287–302,
https://doi.org/10.3354/ame01377, 2010.
Becker, S., Tebben, J., Coffinet, S., Wiltshire, K., Iversen, M. H., Harder,
T., Hinrichs, K. U., and 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.
Beier, S., Rivers, A. R., Moran, M. A., and Obernosterer, I.: The
transcriptional response of prokaryotes to phytoplankton-derived dissolved
organic matter in seawater, Environ. Microbiol., 17, 3466–3480,
https://doi.org/10.1111/1462-2920.12434, 2015.
Benner, R. and Amon, R. M.: The size-reactivity continuum of major
bioelements in the ocean, Annu. Rev. Mar. Sci., 7, 185–205,
https://doi.org/10.1146/annurev-marine-010213-135126, 2015.
Benner, R., Biddanda, B., Black, B., and McCarthy, M.: Abundance, size
distribution, and stable carbon and nitrogen isotopic compositions of marine
organic matter isolated by tangential-flow ultrafiltration, Mar. Chem.,
57, 243–263, https://doi.org/10.1016/S0304-4203(97)00013-3, 1997.
Bolyen, E., Rideout, J. R., Dillon, M. R., Bokulich, N. A., Abnet, C.,
Al-Ghalith, G. A., Alexander, H., Alm, E. J., Arumugam, M., Asnicar, F., and Bai, Y.: Reproducible, interactive, scalable and
extensible microbiome data using QIIME 2, Nat. Biotechnol., 37, 852–857,
https://doi.org/10.1038/s41587-019-0209-9, 2019.
Broek, T. A., Walker, B. D., Guilderson, T. P., Vaughn, J. S., Mason, H. E., and McCarthy, M. D.: Low molecular weight dissolved organic carbon: aging,
compositional changes, and selective utilization during global ocean
circulation, Global Biogeochem. Cy., 34, e2020GB006547,
https://doi.org/10.1029/2020GB006547, 2020.
Callahan, B. J., McMurdie, P. J., Rosen, M. J., Han, A. W., Johnson, A. J.
A., and Holmes, S. P.: DADA2: high-resolution sample inference from
Illumina amplicon data, Nat. Methods, 13, 581–583, https://doi.org/10.1038/nmeth.3869, 2016.
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., and Chisholm, S. W.: Community genomics among
stratified microbial assemblages in the ocean's interior, Science,
311, 496–503, https://doi.org/10.1126/science.1120250, 2006.
Fuhrman, J. A., Cram, J. A., and Needham, D. M.: Marine microbial community
dynamics and their ecological interpretation, Nat. Rev. Microbiol., 13,
133–146, https://doi.org/10.1038/nmeth.3869, 2015.
Guerrero-Feijóo, E., Nieto-Cid, M., Sintes, E., Dobal-Amador, V.,
Hernando-Morales, V., Álvarez, M., Balagué, V., and Varela, M. M.: Optical
properties of dissolved organic matter relate to different depth-specific
patterns of archaeal and bacterial community structure in the North Atlantic
Ocean, FEMS Microbiol. Ecol., 93, fiw224, https://doi.org/10.1093/femsec/fiw224, 2016.
Hartley, B., Barber, H. G., Carter, J. R., and Sims, P. A.: An atlas of British
diatoms, Balogh Scientific Books, ISBN 9780948737459,
1996.
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 particlesm, Nature 409, 801–804, 2001.
Heiderich, 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.
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.
Hoarfrost, A., Balmonte, J. P., Ghobrial, S., Ziervogel, K., Bane, J.,
Gawarkiewicz, G., and Arnosti, C.: Gulf Stream ring water intrusion on the
Mid-Atlantic Bight continental shelf break affects microbially-driven carbon
cycling, Front. Mar. Sci., 6, 394, https://doi.org/10.3389/fmars.2019.00394, 2019.
Hoppe, H. G.: Significance of exoenzymatic activities in the ecology of
brackish water: measurements by means of methylumbelliferyl-substrates,
Marine Ecol.-Prog. Ser., 11, 299–308, https://www.jstor.org/stable/44634717 (last access: 28 November 2022),
1983.
Kaiser, K. and Benner, R.: Organic matter transformations in the upper
mesopelagic zone of the North Pacific: Chemical composition and linkages to
microbial community structure, J. Geophys. Res.-Oceans, 117, C01023,
https://doi.org/10.1029/2011JC007141, 2012.
Kirchman, D.: Measuring bacterial biomass production and growth rates from
leucine incorporation in natural aquatic environments, Method Microbiol.,
30, 227–237, https://doi.org/10.1016/S0580-9517(01)30047-8, 2001.
Kirchman, D., K'Nees, E., and Hodson, R.: Leucine incorporation and its
potential as a measure of protein synthesis by bacteria in natural aquatic
systems, Appl. Environ. Microb., 49, 599–607,
https://doi.org/10.1128/aem.49.3.599-607.1985, 1985.
Li, D. X., Zhang, H., Chen, X. H., Xie, Z. X., Zhang, Y., Zhang, S. F., Lin, L., Chen, F., and Wang, D. Z.: Metaproteomics reveals major microbial players and their
metabolic activities during the blooming period of a marine dinoflagellate
Prorocentrum donghaiense, Environ. Microbiol., 20, 632–644,
https://doi.org/10.1111/1462-2920.13986, 2018.
Luria, C. M., Amaral-Zettler, L. A., Ducklow, H. W., Repeta, D. J., Rhyne,
A. L., and Rich, J. J.: Seasonal shifts in bacterial community responses to
phytoplankton-derived dissolved organic matter in the Western Antarctic
Peninsula, Front. Microbiol., 8, 2117, https://doi.org/10.3389/fmicb.2017.02117, 2017.
Martin, M.: Cutadapt removes adapter sequences from high-throughput
sequencing reads, EMBnet J., 17, 1–10, 2011.
McMurdie, P. J. and Holmes, S.: phyloseq: An R package for reproducible
interactive analysis and graphics of microbiome census data, PloS one, 8,
e61217, https://doi.org/10.1371/journal.pone.0061217, 2013.
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.
Oksanen, J., Blanchet, F. G., Friendly, M., Kindt, R., Legendre, P.,
McGlinn, D., Minchin, P. R., O'Hara, R. B., Simpson, G. L., Solymos, R.,
Stevens, M. H. H., Szoecs, E., Wagner, H.: vegan: Community Ecology Package,
R package version 2.4-6, https://CRAN.R-project.org/package=vegan, last access: 24 August 2018.
Pinheiro, J., Bates, D., DebRoy, S., Sarkar, D., and R Core Team: nlme: Linear and
Nonlinear Mixed Effects Models, R package version 3.1-137, https://CRAN.R-project.org/package=nlme, last access: 24 August 2018.
Poff, K. 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.-Biol., 118, e2018269118, https://doi.org/10.1073/pnas.2018269118, 2021.
Pruesse, E., Quast, C., Knittel, K., Fuchs, B. M., Ludwig, W., Peplies, J.,
and Glöckner, F. O.: SILVA: a comprehensive online resource for quality
checked and aligned ribosomal RNA sequence data compatible with ARB, Nucleic
Acids Res., 35, 7188–7196, https://doi.org/10.1093/nar/gkm864, 2007.
R Core Team: R: A language and environment for statistical computing, R
Foundation for Statistical Computing, Vienna, Austria, https://www.R-project.org/ (last access: 12 October 2022), 2017.
Rognes, T., Flouri, T., Nichols, B., Quince, C., and Mahé, F.: VSEARCH: a versatile open source tool for metagenomics, PeerJ, 4, e2584, https://doi.org/10.7717/peerj.2584, 2016.
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., and Duarte, C. 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.
Saw, J. H., Nunoura, T., Hirai, M., Takaki, Y., Parsons, R., Michelsen, M., Longnecker, K., Kujawinski, E. B., Stepanauskas, R., Landry, Z., and Carlson, C. A.: Pangenomics Analysis Reveals Diversification of
Enzyme Families and Niche Specialization in Globally Abundant SAR202
Bacteria, mBio, 11, e02975-19, https://doi.org/10.1128/mBio.02975-19, 2020.
Sebastián, M., Estrany, M., Ruiz-González, C., Forn, I., Sala, M.
M., Gasol, J. M., and Marrasé, C.: High growth potential of long-term
starved deep ocean opportunistic heterotrophic bacteria, Front. Microbiol.,
10, 760, https://doi.org/10.3389/fmicb.2019.00760, 2019.
Sebastián, M., Forn, I., Auladell, A., Gómez-Letona, M., Sala, M.
M., Gasol, J. M., and Marrasé, C.: Differential recruitment of
opportunistic taxa leads to contrasting abilities in carbon processing by
bathypelagic and surface microbial communities, Environ. Microbiol., 23,
190–206, https://doi.org/10.1111/1462-2920.15292, 2021.
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. Microbiol., 5,
1026–1039, https://doi.org/10.1038/s41564-020-0720-2,
2020.
Simon, M. and Azam, F.: Protein content and protein synthesis rates of
planktonic marine bacteria, Mar. Ecol.-Prog. Ser., 51, 201–213, 1989.
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, 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/ame01755, 2015.
Sunagawa, S., Coelho, L. P., Chaffron, S., Kultima, J. R., Labadie, K., Salazar, G., Djahanschiri, B., Zeller, G., Mende, D. R., Alberti, A., and Cornejo-Castillo, F. M.: Structure and function of the
global ocean microbiome, Science, 348, 1261359,
https://doi.org/10.1126/science.1261359, 2015.
Talley, L. D.: Descriptive physical oceanography: an introduction, Academic
Press, https://doi.org/10.1016/C2009-0-24322-4, 2011.
Teeling, H., Fuchs, B. M., Becher, D., Klockow, C., Gardebrecht, A., Bennke, C. M., Kassabgy, M., Huang, S., Mann, A. J., Waldmann, J., and Weber, M.: Substrate-controlled succession of marine
bacterioplankton populations induced by a phytoplankton bloom, Science,
336, 608–611, https://doi.org/10.1126/science.1218344, 2012.
Traving, S. J., Thygesen, U. H., Riemann, L., and Stedmon, C. A.: A model
of extracellular enzymes in free-living microbes: which strategy pays off?,
Appl. Environ. Microb., 81, 7385–7393, https://doi.org/10.1128/AEM.02070-15, 2015.
Vidal-Melgosa, S., Sichert, A., Francis, T. B., Bartosik, D., Niggemann, J., Wichels, A., Willats, W. G., Fuchs, B. M., Teeling, H., Becher, D., and Schweder, T.: Diatom fucan polysaccharide
precipitates carbon during algal blooms. Nat. Commun., 12, 1–13,
https://doi.org/10.1038/s41467-021-21009-6, 2021.
Wakeham, S. G., Lee, C., Hedges, J. I., Hernes, P. J., and Peterson, M. J.:
Molecular indicators of diagenetic status in marine organic matter, Geochim.
Cosmochim. Ac., 61, 5363–5369, https://doi.org/10.1016/S0016-7037(97)00312-8, 1997.
Wegner, C.-E., Richter-Heitmann, T., Klindworth, A., Klockow, C.,
Richter, M., Achstetter, T., Glockner, F. O., and Harder, J.: Expression of sulfatases in Rhodopirellula baltica and the diversity of sulfatases in the genus Rhodopirellula, Mar. Genom., 9, 51–61, https://doi.org/10.1016/j.margen.2012.12.001, 2013.
Weiss, M. S., Abele, U., Weckesser, J., Welte, W. U., Schiltz, E., and
Schulz, G. E.: Molecular architecture and electrostatic properties of a
bacterial porin, Science, 254, 1627–1630, https://doi.org/10.1126/science.1721242,
1991.
Xing, P., Hahnke, R. L., Unfried, F., Markert, S., Huang, S., Barbeyron, T., Harder, J., Becher, D., Schweder, T., Glöckner, F. O., and Amann, R. I.: Niches of two polysaccharide-degrading Polaribacter
isolates from the North Sea during a spring diatom bloom, ISME J., 9,
1410, https://doi.org/10.1038/ismej.2014.225, 2015.
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.
Bacteria use extracellular enzymes to cut large organic matter to sizes small enough for uptake....
Altmetrics
Final-revised paper
Preprint