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Title: High pCO 2-induced exopolysaccharide-rich ballasted aggregates of planktonic cyanobacteria could explain Paleoproterozoic carbon burial

Abstract

Here, the contribution of planktonic cyanobacteria to burial of organic carbon in deep-sea sediments before the emergence of eukaryotic predators ~1.5 Ga has been considered negligible owing to the slow sinking speed of their small cells. However, global, highly positive excursion in carbon isotope values of inorganic carbonates ~2.22–2.06 Ga implies massive organic matter burial that had to be linked to oceanic cyanobacteria. Here to elucidate that link, we experiment with unicellular planktonic cyanobacteria acclimated to high partial CO 2 pressure ( pCO 2) representative of the early Paleoproterozoic. We find that high pCO 2 boosts generation of acidic extracellular polysaccharides (EPS) that adsorb Ca and Mg cations, support mineralization, and aggregate cells to form ballasted particles. The down flux of such self-assembled cyanobacterial aggregates would decouple the oxygenic photosynthesis from oxidative respiration at the ocean scale, drive export of organic matter from surface to deep ocean and sustain oxygenation of the planetary surface.

Authors:
 [1];  [2];  [2];  [2];  [3];  [2];  [2]; ORCiD logo [2];  [4]
  1. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States); Tel Aviv Univ., Tel Aviv (Israel)
  2. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
  3. Univ. of California, Berkeley, CA (United States)
  4. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States); Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
Publication Date:
Research Org.:
Energy Frontier Research Centers (EFRC) (United States). Center for Nanoscale Control of Geologic CO2 (NCGC); Pacific Northwest National Lab. (PNNL), Richland, WA (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22)
OSTI Identifier:
1441217
Alternate Identifier(s):
OSTI ID: 1460334; OSTI ID: 1558183
Report Number(s):
PNNL-SA-131327
Journal ID: ISSN 2041-1723; PII: 4588
Grant/Contract Number:  
AC05-76RL01830; AC02-05CH11231
Resource Type:
Accepted Manuscript
Journal Name:
Nature Communications
Additional Journal Information:
Journal Volume: 9; Journal Issue: 1; Journal ID: ISSN 2041-1723
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Kamennaya, Nina A., Zemla, Marcin, Mahoney, Laura, Chen, Liang, Holman, Elizabeth, Holman, Hoi -Ying, Auer, Manfred, Ajo-Franklin, Caroline M., and Jansson, Christer. High pCO2-induced exopolysaccharide-rich ballasted aggregates of planktonic cyanobacteria could explain Paleoproterozoic carbon burial. United States: N. p., 2018. Web. doi:10.1038/s41467-018-04588-9.
Kamennaya, Nina A., Zemla, Marcin, Mahoney, Laura, Chen, Liang, Holman, Elizabeth, Holman, Hoi -Ying, Auer, Manfred, Ajo-Franklin, Caroline M., & Jansson, Christer. High pCO2-induced exopolysaccharide-rich ballasted aggregates of planktonic cyanobacteria could explain Paleoproterozoic carbon burial. United States. doi:10.1038/s41467-018-04588-9.
Kamennaya, Nina A., Zemla, Marcin, Mahoney, Laura, Chen, Liang, Holman, Elizabeth, Holman, Hoi -Ying, Auer, Manfred, Ajo-Franklin, Caroline M., and Jansson, Christer. Tue . "High pCO2-induced exopolysaccharide-rich ballasted aggregates of planktonic cyanobacteria could explain Paleoproterozoic carbon burial". United States. doi:10.1038/s41467-018-04588-9. https://www.osti.gov/servlets/purl/1441217.
@article{osti_1441217,
title = {High pCO2-induced exopolysaccharide-rich ballasted aggregates of planktonic cyanobacteria could explain Paleoproterozoic carbon burial},
author = {Kamennaya, Nina A. and Zemla, Marcin and Mahoney, Laura and Chen, Liang and Holman, Elizabeth and Holman, Hoi -Ying and Auer, Manfred and Ajo-Franklin, Caroline M. and Jansson, Christer},
abstractNote = {Here, the contribution of planktonic cyanobacteria to burial of organic carbon in deep-sea sediments before the emergence of eukaryotic predators ~1.5 Ga has been considered negligible owing to the slow sinking speed of their small cells. However, global, highly positive excursion in carbon isotope values of inorganic carbonates ~2.22–2.06 Ga implies massive organic matter burial that had to be linked to oceanic cyanobacteria. Here to elucidate that link, we experiment with unicellular planktonic cyanobacteria acclimated to high partial CO2 pressure (pCO2) representative of the early Paleoproterozoic. We find that high pCO2 boosts generation of acidic extracellular polysaccharides (EPS) that adsorb Ca and Mg cations, support mineralization, and aggregate cells to form ballasted particles. The down flux of such self-assembled cyanobacterial aggregates would decouple the oxygenic photosynthesis from oxidative respiration at the ocean scale, drive export of organic matter from surface to deep ocean and sustain oxygenation of the planetary surface.},
doi = {10.1038/s41467-018-04588-9},
journal = {Nature Communications},
number = 1,
volume = 9,
place = {United States},
year = {2018},
month = {5}
}

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    Works referencing / citing this record:

    Geological constraints on the origin of oxygenic photosynthesis
    journal, September 2010

    • Farquhar, James; Zerkle, Aubrey L.; Bekker, Andrey
    • Photosynthesis Research, Vol. 107, Issue 1
    • DOI: 10.1007/s11120-010-9594-0

    Processes of carbonate precipitation in modern microbial mats
    journal, October 2009


    The evolution of Earth's biogeochemical nitrogen cycle
    journal, September 2016


    Overview of biopolymer-induced mineralization: What goes on in biofilms?
    journal, February 2010


    High phosphate availability as a possible cause for massive cyanobacterial production of oxygen in the Paleoproterozoic atmosphere
    journal, January 2013

    • Papineau, Dominic; Purohit, Ritesh; Fogel, Marilyn L.
    • Earth and Planetary Science Letters, Vol. 362
    • DOI: 10.1016/j.epsl.2012.11.050

    Estimates of atmospheric CO2 in the Neoarchean–Paleoproterozoic from paleosols
    journal, June 2015


    Precambrian paleosols and atmospheric CO2 levels
    journal, June 2006


    Installing extra bicarbonate transporters in the cyanobacterium Synechocystis sp. PCC6803 enhances biomass production
    journal, May 2015


    Screening of Cyanobacterial Species for Calcification
    journal, October 2004

    • Lee, B. D.; Apel, W. A.; Walton, M. R.
    • Biotechnology Progress, Vol. 20, Issue 5
    • DOI: 10.1021/bp0343561

    Morphological and ecological complexity in early eukaryotic ecosystems
    journal, July 2001

    • Javaux, Emmanuelle J.; Knoll, Andrew H.; Walter, Malcolm R.
    • Nature, Vol. 412, Issue 6842
    • DOI: 10.1038/35083562

    Terminal Proterozoic reorganization of biogeochemical cycles
    journal, July 1995

    • Logan, Graham A.; Hayes, J. M.; Hieshima, Glenn B.
    • Nature, Vol. 376, Issue 6535
    • DOI: 10.1038/376053a0

    Atmospheric carbon dioxide concentrations before 2.2 billion years ago
    journal, December 1995

    • Rye, Rob; Kuo, Phillip H.; Holland, Heinrich D.
    • Nature, Vol. 378, Issue 6557
    • DOI: 10.1038/378603a0

    Ocean productivity before about 1.9 Gyr ago limited by phosphorus adsorption onto iron oxides
    journal, May 2002

    • Bjerrum, Christian J.; Canfield, Donald E.
    • Nature, Vol. 417, Issue 6885
    • DOI: 10.1038/417159a

    Dating the cyanobacterial ancestor of the chloroplast
    journal, March 2010

    • Falcón, Luisa I.; Magallón, Susana; Castillo, Amanda
    • The ISME Journal, Vol. 4, Issue 6
    • DOI: 10.1038/ismej.2010.2

    Dating the rise of atmospheric oxygen
    journal, January 2004

    • Bekker, A.; Holland, H. D.; Wang, P. -L.
    • Nature, Vol. 427, Issue 6970
    • DOI: 10.1038/nature02260

    A lower limit for atmospheric carbon dioxide levels 3.2 billion years ago
    journal, April 2004

    • Hessler, Angela M.; Lowe, Donald R.; Jones, Robert L.
    • Nature, Vol. 428, Issue 6984
    • DOI: 10.1038/nature02471

    Aerobic bacterial pyrite oxidation and acid rock drainage during the Great Oxidation Event
    journal, October 2011

    • Konhauser, Kurt O.; Lalonde, Stefan V.; Planavsky, Noah J.
    • Nature, Vol. 478, Issue 7369
    • DOI: 10.1038/nature10511

    Atmospheric oxygenation three billion years ago
    journal, September 2013

    • Crowe, Sean A.; Døssing, Lasse N.; Beukes, Nicolas J.
    • Nature, Vol. 501, Issue 7468
    • DOI: 10.1038/nature12426

    Isotopic evidence for biological nitrogen fixation by molybdenum-nitrogenase from 3.2 Gyr
    journal, February 2015

    • Stüeken, Eva E.; Buick, Roger; Guy, Bradley M.
    • Nature, Vol. 520, Issue 7549
    • DOI: 10.1038/nature14180

    Atmospheric oxygen regulation at low Proterozoic levels by incomplete oxidative weathering of sedimentary organic carbon
    journal, February 2017

    • Daines, Stuart J.; Mills, Benjamin J. W.; Lenton, Timothy M.
    • Nature Communications, Vol. 8, Issue 1
    • DOI: 10.1038/ncomms14379

    Evidence for oxygenic photosynthesis half a billion years before the Great Oxidation Event
    journal, March 2014

    • Planavsky, Noah J.; Asael, Dan; Hofmann, Axel
    • Nature Geoscience, Vol. 7, Issue 4
    • DOI: 10.1038/ngeo2122

    Modulation of oxygen production in Archaean oceans by episodes of Fe(II) toxicity
    journal, January 2015

    • Swanner, Elizabeth D.; Mloszewska, Aleksandra M.; Cirpka, Olaf A.
    • Nature Geoscience, Vol. 8, Issue 2
    • DOI: 10.1038/ngeo2327

    Fast gapped-read alignment with Bowtie 2
    journal, March 2012

    • Langmead, Ben; Salzberg, Steven L.
    • Nature Methods, Vol. 9, Issue 4
    • DOI: 10.1038/nmeth.1923

    Cyanobacterial-bacterial mat consortia: examining the functional unit of microbial survival and growth in extreme environments
    journal, February 2000


    Sulfur record of rising and falling marine oxygen and sulfate levels during the Lomagundi event
    journal, October 2012

    • Planavsky, N. J.; Bekker, A.; Hofmann, A.
    • Proceedings of the National Academy of Sciences, Vol. 109, Issue 45
    • DOI: 10.1073/pnas.1120387109

    Complementary Chromatic Adaptation in a Filamentous Blue-Green alga
    journal, August 1973


    Identifying bacterial genes and endosymbiont DNA with Glimmer
    journal, January 2007


    Trimmomatic: a flexible trimmer for Illumina sequence data
    journal, April 2014


    HTSeq--a Python framework to work with high-throughput sequencing data
    journal, September 2014


    CO2 concentrating mechanisms in cyanobacteria: molecular components, their diversity and evolution
    journal, February 2003

    • Badger, M. R.
    • Journal of Experimental Botany, Vol. 54, Issue 383
    • DOI: 10.1093/jxb/erg076

    The Pfam protein families database
    journal, November 2011

    • Punta, M.; Coggill, P. C.; Eberhardt, R. Y.
    • Nucleic Acids Research, Vol. 40, Issue D1
    • DOI: 10.1093/nar/gkr1065

    Algal evolution in relation to atmospheric CO 2 : carboxylases, carbon-concentrating mechanisms and carbon oxidation cycles
    journal, February 2012

    • Raven, John A.; Giordano, Mario; Beardall, John
    • Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 367, Issue 1588
    • DOI: 10.1098/rstb.2011.0212

    Velvet: Algorithms for de novo short read assembly using de Bruijn graphs
    journal, February 2008


    The Regulation of Photosynthetic Structure and Function during Nitrogen Deprivation in Chlamydomonas reinhardtii
    journal, December 2014

    • Juergens, Matthew T.; Deshpande, Rahul R.; Lucker, Ben F.
    • Plant Physiology, Vol. 167, Issue 2
    • DOI: 10.1104/pp.114.250530

    Selectivity in the heavy metal removal by exopolysaccharide-producing cyanobacteria
    journal, July 2008


    A widespread positive ? 13 C carb anomaly at around 2.33?2.06 Ga on the Fennoscandian Shield: a paradox?
    journal, March 1996


    Bioenergetic changes in the microalgal photosynthetic apparatus by extremely high CO 2 concentrations induce an intense biomass production
    journal, March 2008


    Cyanobacteria and the Great Oxidation Event: evidence from genes and fossils
    journal, June 2015

    • Schirrmeister, Bettina E.; Gugger, Muriel; Donoghue, Philip C. J.
    • Palaeontology, Vol. 58, Issue 5
    • DOI: 10.1111/pala.12178

    EVOLUTION: Tracing Oxygen's Imprint on Earth's Metabolic Evolution
    journal, March 2006


    Earth's early atmosphere
    journal, February 1993


    Earth and Mars: Evolution of Atmospheres and Surface Temperatures
    journal, July 1972


    Redox Stabilization of the Atmosphere and Oceans by Phosphorus-Limited Marine Productivity
    journal, January 1996


    Evolution of a Habitable Planet
    journal, September 2003


    THE EARLY HISTORY OF ATMOSPHERIC OXYGEN: Homage to Robert M. Garrels
    journal, May 2005


    Accelerated Profile HMM Searches
    journal, October 2011


    Role of Cyanobacterial Exopolysaccharides in Phototrophic Biofilms and in Complex Microbial Mats
    journal, April 2015


    Cyanobacteria as Biocatalysts for Carbonate Mineralization
    journal, October 2012

    • Kamennaya, Nina; Ajo-Franklin, Caroline; Northen, Trent
    • Minerals, Vol. 2, Issue 4
    • DOI: 10.3390/min2040338