Cyanobacterial reuse of extracellular organic carbon in microbial mats

Stuart, Rhona K.; Mayali, Xavier; Lee, Jackson Z.; Craig Everroad, R.; Hwang, Mona; Bebout, Brad M.; Weber, Peter K.; Pett-Ridge, Jennifer; Thelen, Michael P.

doi:10.1038/ismej.2015.180

Title: Cyanobacterial reuse of extracellular organic carbon in microbial mats

Journal Article · Fri Oct 23 00:00:00 EDT 2015 · The ISME Journal

DOI:https://doi.org/10.1038/ismej.2015.180· OSTI ID:1623770

Stuart, Rhona K. ^[1]; Mayali, Xavier ^[1]; Lee, Jackson Z. ^[2]; Craig Everroad, R. ^[2]; Hwang, Mona ^[1]; Bebout, Brad M. ^[2]; Weber, Peter K. ^[1]; Pett-Ridge, Jennifer ^[1];

^[1]

Lawrence Livermore National Lab. (LLNL), Livermore, CA (United States), Physical and Life Sciences Directorate
NASA Ames Research Center (ARC), Moffett Field, Mountain View, CA (United States), Exobiology Branch

Cyanobacterial organic matter excretion is crucial to carbon cycling in many microbial communities, but the nature and bioavailability of this C depend on unknown physiological functions. Cyanobacteria-dominated hypersaline laminated mats are a useful model ecosystem for the study of C flow in complex communities, as they use photosynthesis to sustain a more or less closed system. Although such mats have a large C reservoir in the extracellular polymeric substances (EPSs), the production and degradation of organic carbon is not well defined. To identify extracellular processes in cyanobacterial mats, we examined mats collected from Elkhorn Slough (ES) at Monterey Bay, California, for glycosyl and protein composition of the EPS. We found a prevalence of simple glucose polysaccharides containing either α or β (1,4) linkages, indicating distinct sources of glucose with differing enzymatic accessibility. Using proteomics, we identified cyanobacterial extracellular enzymes, and also detected activities that indicate a capacity for EPS degradation. In a less complex system, we characterized the EPS of a cyanobacterial isolate from ES, ESFC-1, and found the extracellular composition of biofilms produced by this unicyanobacterial culture were similar to that of natural mats. By tracing isotopically labeled EPS into single cells of ESFC-1, we demonstrated rapid incorporation of extracellular-derived carbon. Taken together, these results indicate cyanobacteria reuse excess organic carbon, constituting a dynamic pool of extracellular resources in these mats.

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Research Organization:: Lawrence Livermore National Laboratory (LLNL), Livermore, CA (United States); Univ. of Georgia, Athens, GA (United States)

Sponsoring Organization:: USDOE

Grant/Contract Number:: AC52-07NA27344; FG02-93ER20097

OSTI ID:: 1623770

Journal Information:: The ISME Journal, Vol. 10, Issue 5; ISSN 1751-7362

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 75 works

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References (54)

The Anabaena sp. PCC 7120 Exoproteome: Taking a Peek outside the Box Oliveira, Paulo; Martins, Nuno; Santos, Marina Life, Vol. 5, Issue 1 https://doi.org/10.3390/life5010130	journal	January 2015
Characterization and Biological Implications of Scytonemin, a Cyanobacterial Sheath Pigment1 Garcia-Pichel, Ferran; Castenholz, Richard W. Journal of Phycology, Vol. 27, Issue 3 https://doi.org/10.1111/j.0022-3646.1991.00395.x	journal	June 1991
Active Fe-Containing Superoxide Dismutase and Abundant sodF mRNA in Nostoc commune(Cyanobacteria) after Years of Desiccation Shirkey, Breanne; Kovarcik, Don Paul; Wright, Deborah J. Journal of Bacteriology, Vol. 182, Issue 1 https://doi.org/10.1128/JB.182.1.189-197.2000	journal	January 2000
Comparative ecology of H2 cycling in sedimentary and phototrophic ecosystems Hoehler, Tori M.; Albert, Daniel B.; Alperin, Marc J. Antonie van Leeuwenhoek, Vol. 81, Issue 1/4, p. 575-585 https://doi.org/10.1023/A:1020517924466	journal	January 2002
The effect of solar UV and visible irradiance on the vertical movements of cyanobacteria in microbial mats of hypersaline waters Kruschel, Claudia; Castenholz, Richard W. FEMS Microbiology Ecology, Vol. 27, Issue 1 https://doi.org/10.1111/j.1574-6941.1998.tb00525.x	journal	September 1998
Exocellular polysaccharides from cyanobacteria and their possible applications De Philippis, Roberto; Vincenzini, Massimo FEMS Microbiology Reviews, Vol. 22, Issue 3 https://doi.org/10.1111/j.1574-6976.1998.tb00365.x	journal	September 1998
Photoheterotrophy in marine prokaryotes Zubkov, M. V. Journal of Plankton Research, Vol. 31, Issue 9 https://doi.org/10.1093/plankt/fbp043	journal	June 2009
Glucose Uptake and Its Effect on Gene Expression in Prochlorococcus Gómez-Baena, Guadalupe; López-Lozano, Antonio; Gil-Martínez, Jorge PLoS ONE, Vol. 3, Issue 10 https://doi.org/10.1371/journal.pone.0003416	journal	October 2008
A Colorimetric Method for the Determination of Sugars Dubois, M.; Gilles, K.; Hamilton, J. K. Nature, Vol. 168, Issue 4265 https://doi.org/10.1038/168167a0	journal	July 1951
Cellulose in Cyanobacteria. Origin of Vascular Plant Cellulose Synthase? Nobles, David R.; Romanovicz, Dwight K.; Brown, R. Malcolm Plant Physiology, Vol. 127, Issue 2 https://doi.org/10.1104/pp.010557	journal	October 2001
Bacterial Growth Efficiency in Natural Aquatic Systems del Giorgio, Paul A.; Cole, Jonathan J. Annual Review of Ecology and Systematics, Vol. 29, Issue 1 https://doi.org/10.1146/annurev.ecolsys.29.1.503	journal	November 1998
The role of microbial mats in the production of reduced gases on the early Earth Hoehler, Tori M.; Bebout, Brad M.; Des Marais, David J. Nature, Vol. 412, Issue 6844 https://doi.org/10.1038/35085554	journal	July 2001
Mechanisms of intrinsic resistance to antimicrobial peptides of Edwardsiella ictaluri and its influence on fish gut inflammation and virulence Gatlin, Delbert M.; Santander, Javier; Loh, Amanda Microbiology, Vol. 159, Issue 7 https://doi.org/10.1099/mic.0.066639-0	journal	July 2013
Untargeted metabolic footprinting reveals a surprising breadth of metabolite uptake and release by Synechococcus sp. PCC 7002 Baran, Richard; Bowen, Benjamin P.; Northen, Trent R. Molecular BioSystems, Vol. 7, Issue 12 https://doi.org/10.1039/c1mb05196b	journal	January 2011
Diel rhythmicity in amino acid uptake by Prochlorococcus Mary, Isabelle; Garczarek, Laurence; Tarran, Glen A. Environmental Microbiology, Vol. 10, Issue 8 https://doi.org/10.1111/j.1462-2920.2008.01633.x	journal	August 2008
The use of DAPI for identifying and counting aquatic microflora1 Porter, Karen G.; Feig, Yvette S. Limnology and Oceanography, Vol. 25, Issue 5 https://doi.org/10.4319/lo.1980.25.5.0943	journal	September 1980
Identification of a novel cyanobacterial group as active diazotrophs in a coastal microbial mat using NanoSIMS analysis Woebken, Dagmar; Burow, Luke C.; Prufert-Bebout, Leslie The ISME Journal, Vol. 6, Issue 7 https://doi.org/10.1038/ismej.2011.200	journal	January 2012
Fermentation in cyanobacteria Stal, L. FEMS Microbiology Reviews, Vol. 21, Issue 2 https://doi.org/10.1016/S0168-6445(97)00056-9	journal	September 1997
The structure of Cryptococcus neoformans galactoxylomannan contains β-d-glucuronic acid Heiss, Christian; Stacey Klutts, J.; Wang, Zhirui Carbohydrate Research, Vol. 344, Issue 7 https://doi.org/10.1016/j.carres.2009.03.003	journal	May 2009
The biofilm matrix Flemming, Hans-Curt; Wingender, Jost Nature Reviews Microbiology, Vol. 8, Issue 9 https://doi.org/10.1038/nrmicro2415	journal	August 2010
Molecular biology of cyanobacterial salt acclimation Hagemann, Martin FEMS Microbiology Reviews, Vol. 35, Issue 1 https://doi.org/10.1111/j.1574-6976.2010.00234.x	journal	January 2011
Processes of carbonate precipitation in modern microbial mats Dupraz, Christophe; Reid, R. Pamela; Braissant, Olivier Earth-Science Reviews, Vol. 96, Issue 3 https://doi.org/10.1016/j.earscirev.2008.10.005	journal	October 2009
Anoxic carbon flux in photosynthetic microbial mats as revealed by metatranscriptomics Burow, Luke C.; Woebken, Dagmar; Marshall, Ian PG The ISME Journal, Vol. 7, Issue 4 https://doi.org/10.1038/ismej.2012.150	journal	November 2012
Nostoc (Cyanophyceae) goes Nude: Extracellular Polysaccharides Serve as a sink for Reducing Power Under Unbalanced c/n Metabolism1: eps Synthesis and Function in Nostoc Otero, Ana; Vincenzini, Massimo Journal of Phycology, Vol. 40, Issue 1 https://doi.org/10.1111/j.0022-3646.2003.03-067.x	journal	January 2004
Carbon and nitrogen fixation and metabolite exchange in and between individual cells of Anabaena oscillarioides Popa, Radu; Weber, Peter K.; Pett-Ridge, Jennifer The ISME Journal, Vol. 1, Issue 4 https://doi.org/10.1038/ismej.2007.44	journal	July 2007
The Ecological Significance of Extracellular Products of Phytoplankton Photosynthesis Fogg, G. E. Botanica Marina, Vol. 26, Issue 1 https://doi.org/10.1515/botm.1983.26.1.3	journal	January 1983
Long-Term Manipulations of Intact Microbial Mat Communities in a Greenhouse Collaboratory: Simulating Earth's Present and Past Field Environments Bebout, Brad M.; Carpenter, Steven P.; Des Marais, David J. Astrobiology, Vol. 2, Issue 4 https://doi.org/10.1089/153110702762470491	journal	December 2002
Draft Genome Sequence of an Oscillatorian Cyanobacterium, Strain ESFC-1 Everroad, R. C.; Woebken, D.; Singer, S. W. Genome Announcements, Vol. 1, Issue 4 https://doi.org/10.1128/genomeA.00527-13	journal	June 2013
GROWTH AND CARBON CONTENT OF THREE DIFFERENT-SIZED DIAZOTROPHIC CYANOBACTERIA OBSERVED IN THE SUBTROPICAL NORTH PACIFIC ¹ Goebel, Nicole L.; Edwards, Christopher A.; Carter, Brandon J. Journal of Phycology, Vol. 44, Issue 5 https://doi.org/10.1111/j.1529-8817.2008.00581.x	journal	October 2008
Genome analyses highlight the different biological roles of cellulases Medie, Felix Mba; Davies, Gideon J.; Drancourt, Michel Nature Reviews Microbiology, Vol. 10, Issue 3 https://doi.org/10.1038/nrmicro2729	journal	January 2012
Fixation and fate of C and N in the cyanobacterium Trichodesmium using nanometer-scale secondary ion mass spectrometry Finzi-Hart, J. A.; Pett-Ridge, J.; Weber, P. K. Proceedings of the National Academy of Sciences, Vol. 106, Issue 15 https://doi.org/10.1073/pnas.0810547106	journal	March 2009
Complexity of cyanobacterial exopolysaccharides: composition, structures, inducing factors and putative genes involved in their biosynthesis and assembly Pereira, Sara; Zille, Andrea; Micheletti, Ernesto FEMS Microbiology Reviews, Vol. 33, Issue 5 https://doi.org/10.1111/j.1574-6976.2009.00183.x	journal	September 2009
Phosphonate utilization by the globally important marine diazotroph Trichodesmium Dyhrman, S. T.; Chappell, P. D.; Haley, S. T. Nature, Vol. 439, Issue 7072 https://doi.org/10.1038/nature04203	journal	January 2006
Estimates of global cyanobacterial biomass and its distribution Garcia-Pichel, Ferran; Belnap, Jayne; Neuer, Susanne Algological Studies, Vol. 109, Issue 1 https://doi.org/10.1127/1864-1318/2003/0109-0213	journal	August 2003
Production and cycling of natural microbial exopolymers (EPS) within a marine stromatolite Decho, Alan W.; Visscher, Pieter T.; Reid, R. Pamela Palaeogeography, Palaeoclimatology, Palaeoecology, Vol. 219, Issue 1-2 https://doi.org/10.1016/j.palaeo.2004.10.015	journal	April 2005
Microscale characterization of dissolved organic matter production and uptake in marine microbial mat communities Paerl, Hans W.; Bebout, Brad M.; Joye, Samantha B. Limnology and Oceanography, Vol. 38, Issue 6 https://doi.org/10.4319/lo.1993.38.6.1150	journal	September 1993
Characterization of Extracellular Polymeric Substances from Acidophilic Microbial Biofilms Jiao, Y.; Cody, G. D.; Harding, A. K. Applied and Environmental Microbiology, Vol. 76, Issue 9 https://doi.org/10.1128/AEM.02289-09	journal	March 2010
Extracellular polymeric substances (EPS) from cyanobacterial mats: characterisation and isolation method optimisation Klock, Jan-Hendrik; Wieland, Andrea; Seifert, Richard Marine Biology, Vol. 152, Issue 5 https://doi.org/10.1007/s00227-007-0754-5	journal	July 2007
Competition for sulfide among colorless and purple sulfur bacteria in cyanobacterial mats Jørgensen, B. FEMS Microbiology Letters, Vol. 38, Issue 3 https://doi.org/10.1016/0378-1097(86)90049-2	journal	August 1986
Microelectrode studies of the photosynthesis and O ₂ , H ₂ S, and pH profiles of a microbial mat1: O ₂ , H ₂ S, and pH in microbial mat Revsbech, Niels Peter; Jorgensen, Bo Barker; Blackburn, T. Henry Limnology and Oceanography, Vol. 28, Issue 6 https://doi.org/10.4319/lo.1983.28.6.1062	journal	November 1983
Osmotic shock-induced release of low molecular weight metabolites from free-living and immobilized cyanobacteria Reed, Robert H.; Warr, Stephen R. C.; Kerby, Nigel W. Enzyme and Microbial Technology, Vol. 8, Issue 2 https://doi.org/10.1016/0141-0229(86)90080-3	journal	February 1986
Physical characterization and diel dynamics of different fractions of extracellular polysaccharides in an axenic culture of a benthic diatom De Brouwer, J. F. C.; Wolfstein, K.; Stal, L. J. European Journal of Phycology, Vol. 37, Issue 1 https://doi.org/10.1017/S0967026201003419	journal	February 2002
The exo-proteome and exo-metabolome of Nostoc punctiforme (Cyanobacteria) in the presence and absence of nitrate Vilhauer, Laura; Jervis, Judith; Ray, W. Keith Archives of Microbiology, Vol. 196, Issue 5 https://doi.org/10.1007/s00203-014-0974-2	journal	March 2014
Hydrogen production in photosynthetic microbial mats in the Elkhorn Slough estuary, Monterey Bay Burow, Luke C.; Woebken, Dagmar; Bebout, Brad M. The ISME Journal, Vol. 6, Issue 4 https://doi.org/10.1038/ismej.2011.142	journal	October 2011
Crinalium epipsammum sp. nov.: a filamentous cyanobacterium with trichomes composed of elliptical cells and containing poly- -(1,4) glucar (cellulose) de Winder, B.; Stal, L. J.; Mur, L. R. Journal of General Microbiology, Vol. 136, Issue 8 https://doi.org/10.1099/00221287-136-8-1645	journal	August 1990
UV Irradiation and Desiccation Modulate the Three-dimensional Extracellular Matrix of Nostoc commune (Cyanobacteria) Wright, Deborah J.; Smith, Sue C.; Joardar, Vinita Journal of Biological Chemistry, Vol. 280, Issue 48 https://doi.org/10.1074/jbc.M505961200	journal	September 2005
Diel Interactions of Oxygenic Photosynthesis and N2 Fixation (Acetylene Reduction) in a Marine Microbial Mat Community Bebout, Brad M.; Paerl, Hans W.; Crocker, Kenneth M. Applied and Environmental Microbiology, Vol. 53, Issue 10 https://doi.org/10.1128/AEM.53.10.2353-2362.1987	journal	January 1987
Competition for sulfide among colorless and purple sulfur bacteria in cyanobacterial mats JÃ¸rgensen, Bo Barker; Marais, David J. FEMS Microbiology Letters, Vol. 38, Issue 3 https://doi.org/10.1111/j.1574-6968.1986.tb01727.x	journal	August 1986
Bacterial Biovolume and Biomass Estimations Bratbak, Gunnar Applied and Environmental Microbiology, Vol. 49, Issue 6 https://doi.org/10.1128/aem.49.6.1488-1493.1985	journal	January 1985
Occurrence of UV-Absorbing, Mycosporine-Like Compounds among Cyanobacterial Isolates and an Estimate of Their Screening Capacity Garcia-Pichel, Ferran; Castenholz, Richard W. Applied and Environmental Microbiology, Vol. 59, Issue 1 https://doi.org/10.1128/aem.59.1.163-169.1993	journal	January 1993
Diel Migrations of Microorganisms within a Benthic, Hypersaline Mat Community Garcia-Pichel, Ferran; Mechling, Margaret; Castenholz, Richard W. Applied and Environmental Microbiology, Vol. 60, Issue 5 https://doi.org/10.1128/aem.60.5.1500-1511.1994	journal	January 1994
Crucial Role of Extracellular Polysaccharides in Desiccation and Freezing Tolerance in the Terrestrial Cyanobacterium Nostoc commune Tamaru, Y.; Takani, Y.; Yoshida, T. Applied and Environmental Microbiology, Vol. 71, Issue 11 https://doi.org/10.1128/aem.71.11.7327-7333.2005	journal	November 2005
SwmB, a 1.12-Megadalton Protein That Is Required for Nonflagellar Swimming Motility in Synechococcus McCarren, J.; Brahamsha, B. Journal of Bacteriology, Vol. 189, Issue 3 https://doi.org/10.1128/jb.01500-06	journal	December 2006
Fermentation couples Chloroflexi and sulfate-reducing bacteria to Cyanobacteria in hypersaline microbial mats Lee, Jackson Z.; Burow, Luke C.; Woebken, Dagmar Frontiers in Microbiology, Vol. 5 https://doi.org/10.3389/fmicb.2014.00061	journal	January 2014

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