Temporal succession in carbon incorporation from macromolecules by particle-attached bacteria in marine microcosms: Particle-attached bacteria incorporating organic carbon

Mayali, Xavier; Stewart, Benjamin; Mabery, Shalini; Weber, Peter K.

doi:10.1111/1758-2229.12352

Title: Temporal succession in carbon incorporation from macromolecules by particle-attached bacteria in marine microcosms: Particle-attached bacteria incorporating organic carbon

Journal Article · Mon Dec 21 00:00:00 EST 2015 · Environmental Microbiology Reports

DOI:https://doi.org/10.1111/1758-2229.12352· OSTI ID:1248309

Mayali, Xavier ^[1]; Stewart, Benjamin ^[1]; Mabery, Shalini ^[1]; Weber, Peter K. ^[1]

Lawrence Livermore National Lab. (LLNL), Livermore, CA (United States)

Here, we investigated bacterial carbon assimilation from stable isotope-labelled macromolecular substrates (proteins; lipids; and two types of polysaccharides, starch and cellobiose) while attached to killed diatom detrital particles during laboratory microcosms incubated for 17 days. Using Chip-SIP (secondary ion mass spectrometry analysis of RNA microarrays), we identified generalist operational taxonomic units (OTUs) from the Gammaproteobacteria, belonging to the genera Colwellia, Glaciecola, Pseudoalteromonas and Rheinheimera, and from the Bacteroidetes, genera Owenweeksia and Maribacter, that incorporated the four tested substrates throughout the incubation period. Many of these OTUs exhibited the highest isotope incorporation relative to the others, indicating that they were likely the most active. Additional OTUs from the Gammaproteobacteria, Bacteroidetes and Alphaproteobacteria exhibited generally (but not always) lower activity and did not incorporate all tested substrates at all times, showing species succession in organic carbon incorporation. We also found evidence to suggest that both generalist and specialist OTUs changed their relative substrate incorporation over time, presumably in response to changing substrate availability as the particles aged. This pattern was demonstrated by temporal succession from relatively higher starch incorporation early in the incubations, eventually switching to higher cellobiose incorporation after 2 weeks.

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Research Organization:: Lawrence Livermore National Lab. (LLNL), Livermore, CA (United States)

Sponsoring Organization:: USDOE

DOE Contract Number:: AC52-07NA27344

OSTI ID:: 1248309

Report Number(s):: LLNL-JRNL-641031

Journal Information:: Environmental Microbiology Reports, Vol. 8, Issue 1; ISSN 1758-2229

Publisher:: Wiley-Blackwell

Country of Publication:: United States

Language:: English

References (36)

Bacterial control of silicon regeneration from diatom detritus: Significance of bacterial ectohydrolases and species identity Bidle, Kay D.; Azam, Farooq Limnology and Oceanography, Vol. 46, Issue 7 https://doi.org/10.4319/lo.2001.46.7.1606	journal	November 2001
Spatial variability of particle-attached and free-living bacterial diversity in surface waters from the Mackenzie River to the Beaufort Sea (Canadian Arctic) Ortega-Retuerta, E.; Joux, F.; Jeffrey, W. H. Biogeosciences, Vol. 10, Issue 4 https://doi.org/10.5194/bg-10-2747-2013	journal	January 2013
Algae-bacteria interactions and their effects on aggregation and organic matter flux in the sea Grossart, Hans-Peter; Czub, Gertje; Simon, Meinhard Environmental Microbiology, Vol. 8, Issue 6 https://doi.org/10.1111/j.1462-2920.2006.00999.x	journal	June 2006
Succession of Pelagic Marine Bacteria during Enrichment: a Close Look at Cultivation-Induced Shifts Eilers, H.; Pernthaler, J.; Amann, R. Applied and Environmental Microbiology, Vol. 66, Issue 11 https://doi.org/10.1128/AEM.66.11.4634-4640.2000	journal	November 2000
Evidence for microbial attenuation of particle flux in the Amundsen Gulf and Beaufort Sea: elevated hydrolytic enzyme activity on sinking aggregates Kellogg, Colleen T. E.; Carpenter, Shelly D.; Renfro, Alisha A. Polar Biology, Vol. 34, Issue 12 https://doi.org/10.1007/s00300-011-1015-0	journal	May 2011
Linking Microbial Phylogeny to Metabolic Activity at the Single-Cell Level by Using Enhanced Element Labeling-Catalyzed Reporter Deposition Fluorescence In Situ Hybridization (EL-FISH) and NanoSIMS Behrens, S.; Losekann, T.; Pett-Ridge, J. Applied and Environmental Microbiology, Vol. 74, Issue 10 https://doi.org/10.1128/AEM.00191-08	journal	March 2008
Dissolved organic matter assimilation by heterotrophic bacterial groups in the western Arctic Ocean Elifantz, H.; Dittel, Ai; Cottrell, Mt Aquatic Microbial Ecology, Vol. 50 https://doi.org/10.3354/ame01145	journal	December 2007
Contrasting genomic properties of free-living and particle-attached microbial assemblages within a coastal ecosystem Smith, Maria W.; Zeigler Allen, Lisa; Allen, Andrew E. Frontiers in Microbiology, Vol. 4 https://doi.org/10.3389/fmicb.2013.00120	journal	January 2013
Microbial ecology of organic aggregates in aquatic ecosystems Simon, M.; Grossart, Hp; Schweitzer, B. Aquatic Microbial Ecology, Vol. 28 https://doi.org/10.3354/ame028175	journal	January 2002
Intense hydrolytic enzyme activity on marine aggregates and implications for rapid particle dissolution Smith, David C.; Simon, Meinhard; Alldredge, Alice L. Nature, Vol. 359, Issue 6391 https://doi.org/10.1038/359139a0	journal	September 1992
Particle-attached and free-living bacterial communities in a contrasting marine environment: Victoria Harbor, Hong Kong: Particle-attached and free-living bacterial communities Zhang, Rui; Liu, Baozhong; Lau, Stanley C. K. FEMS Microbiology Ecology, Vol. 61, Issue 3 https://doi.org/10.1111/j.1574-6941.2007.00353.x	journal	September 2007
Microbial enzymatic activities and prokaryotic abundance in the upwelling system of the Straits of Messina (Sicily): distribution, dynamics and biogeochemical considerations Caruso, G.; Azzaro, F.; La Ferla, R. Advances in Oceanography and Limnology, Vol. 4, Issue 1 https://doi.org/10.4081/aiol.2013.5336	journal	April 2013
Taxonomic composition of the particle-attached and free-living bacterial assemblages in the Northwest Mediterranean Sea analyzed by pyrosequencing of the 16S rRNA Crespo, Bibiana G.; Pommier, Thomas; Fernández-Gómez, Beatriz MicrobiologyOpen, Vol. 2, Issue 4 https://doi.org/10.1002/mbo3.92	journal	May 2013
Variability in ectohydrolytic enzyme activities of pelagic marine bacteria and its significance for substrate processing in the sea Martinez, J.; Smith, Dc; Steward, Gf Aquatic Microbial Ecology, Vol. 10 https://doi.org/10.3354/ame010223	journal	January 1996
Accelerated dissolution of diatom silica by marine bacterial assemblages Bidle, Kay D.; Azam, Farooq Nature, Vol. 397, Issue 6719 https://doi.org/10.1038/17351	journal	February 1999
Proteogenomic basis for ecological divergence of closely related bacteria in natural acidophilic microbial communities Denef, V. J.; Kalnejais, L. H.; Mueller, R. S. Proceedings of the National Academy of Sciences, Vol. 107, Issue 6 https://doi.org/10.1073/pnas.0907041107	journal	February 2010
Polysaccharide hydrolysis in aggregates and free enzyme activity in aggregate-free seawater from the north-eastern Gulf of Mexico Ziervogel, Kai; Arnosti, Carol Environmental Microbiology, Vol. 10, Issue 2 https://doi.org/10.1111/j.1462-2920.2007.01451.x	journal	February 2008
Sea snow microcosms Azam, Farooq; Long, Richard A. Nature, Vol. 414, Issue 6863 https://doi.org/10.1038/35107174	journal	November 2001
Antagonistic Interactions among Marine Pelagic Bacteria Long, R. A.; Azam, F. Applied and Environmental Microbiology, Vol. 67, Issue 11 https://doi.org/10.1128/AEM.67.11.4975-4983.2001	journal	November 2001
Spatial and Temporal Variations in Chitinolytic Gene Expression and Bacterial Biomass Production during Chitin Degradation Baty, A. M.; Eastburn, C. C.; Techkarnjanaruk, S. Applied and Environmental Microbiology, Vol. 66, Issue 8 https://doi.org/10.1128/AEM.66.8.3574-3585.2000	journal	August 2000
High-throughput isotopic analysis of RNA microarrays to quantify microbial resource use Mayali, Xavier; Weber, Peter K.; Brodie, Eoin L. The ISME Journal, Vol. 6, Issue 6 https://doi.org/10.1038/ismej.2011.175	journal	December 2011
The Isotope Array, a New Tool That Employs Substrate-Mediated Labeling of rRNA for Determination of Microbial Community Structure and Function Adamczyk, J.; Hesselsoe, M.; Iversen, N. Applied and Environmental Microbiology, Vol. 69, Issue 11 https://doi.org/10.1128/AEM.69.11.6875-6887.2003	journal	November 2003
Dynamics of Microbial Communities on Marine Snow Aggregates: Colonization, Growth, Detachment, and Grazing Mortality of Attached Bacteria Kiorboe, T.; Tang, K.; Grossart, H. -P. Applied and Environmental Microbiology, Vol. 69, Issue 6 https://doi.org/10.1128/AEM.69.6.3036-3047.2003	journal	June 2003
Characterization of marine bacteria and the activity of their enzyme systems involved in degradation of the algal storage glucan laminarin: Degradation of the algal glucan laminarin by marine bacteria Alderkamp, Anne-Carlijn; Van Rijssel, Marion; Bolhuis, Henk FEMS Microbiology Ecology, Vol. 59, Issue 1 https://doi.org/10.1111/j.1574-6941.2006.00219.x	journal	January 2007
Contrasting extracellular enzyme activities of particle-associated bacteria from distinct provinces of the North Atlantic Ocean Arnosti, Carol; Fuchs, Bernhard M.; Amann, Rudolf Frontiers in Microbiology, Vol. 3 https://doi.org/10.3389/fmicb.2012.00425	journal	January 2012
Comparison of cell-specific activity between free-living and attached bacteria using isolates and natural assemblages Grossart, Hans-Peter; Tang, Kam W.; KiÃ¸rboe, Thomas FEMS Microbiology Letters, Vol. 266, Issue 2 https://doi.org/10.1111/j.1574-6968.2006.00520.x	journal	January 2007
Composition and degradation of marine particles with different settling velocities in the northwestern Mediterranean Sea Goutx, Madeleine; Wakeham, Stuart G.; Lee, Cindy Limnology and Oceanography, Vol. 52, Issue 4 https://doi.org/10.4319/lo.2007.52.4.1645	journal	July 2007
The biological degradation of cellulose Beguin, Pierre; Aubert, Jean-Paul FEMS Microbiology Reviews, Vol. 13, Issue 1, p. 25-58 https://doi.org/10.1111/j.1574-6976.1994.tb00033.x	journal	January 1994
Comparison of bacterial communities on limnic versus coastal marine particles reveals profound differences in colonization: Marine and limnic particle-associated bacteria Bižić-Ionescu, Mina; Zeder, Michael; Ionescu, Danny Environmental Microbiology, Vol. 17, Issue 10 https://doi.org/10.1111/1462-2920.12466	journal	April 2014
Natural Assemblages of Marine Proteobacteria and Members of the Cytophaga-Flavobacter Cluster Consuming Low- and High-Molecular-Weight Dissolved Organic Matter Cottrell, M. T.; Kirchman, D. L. Applied and Environmental Microbiology, Vol. 66, Issue 4 https://doi.org/10.1128/AEM.66.4.1692-1697.2000	journal	April 2000
Phylogenetic diversity of aggregate-attached vs. free-living marine bacterial assemblages DeLong, Edward F.; Franks, Diana G.; Alldredge, Alice L. Limnology and Oceanography, Vol. 38, Issue 5 https://doi.org/10.4319/lo.1993.38.5.0924	journal	July 1993
Diel and Seasonal Variations in Abundance, Activity, and Community Structure of Particle-Attached and Free-Living Bacteria in NW Mediterranean Sea Ghiglione, J. F.; Mevel, G.; Pujo-Pay, M. Microbial Ecology, Vol. 54, Issue 2 https://doi.org/10.1007/s00248-006-9189-7	journal	March 2007
Diversity of Free-Living and Attached Bacteria in Offshore Western Mediterranean Waters as Depicted by Analysis of Genes Encoding 16S rRNA Acinas, Silvia G.; Antón, Josefa; Rodríguez-Valera, Francisco Applied and Environmental Microbiology, Vol. 65, Issue 2 https://doi.org/10.1128/AEM.65.2.514-522.1999	journal	February 1999
Interaction of ruminal bacteria in the production and utilization of maltooligosaccharides from starch. Cotta, M. A. Applied and Environmental Microbiology, Vol. 58, Issue 1 https://doi.org/10.1128/AEM.58.1.48-54.1992	journal	January 1992
Direct Determination of Carbon and Nitrogen Contents of Natural Bacterial Assemblages in Marine Environments Fukuda, Rumi; Ogawa, Hiroshi; Nagata, Toshi Applied and Environmental Microbiology, Vol. 64, Issue 9 https://doi.org/10.1128/AEM.64.9.3352-3358.1998	journal	September 1998
Combined Microautoradiography–16S rRNA Probe Technique for Determination of Radioisotope Uptake by Specific Microbial Cell Types In Situ Ouverney, Cleber C.; Fuhrman, Jed A. Applied and Environmental Microbiology, Vol. 65, Issue 4 https://doi.org/10.1128/AEM.65.4.1746-1752.1999	journal	April 1999

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