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Title: The Green Berry Consortia of the Sippewissett Salt Marsh: Millimeter-Sized Aggregates of Diazotrophic Unicellular Cyanobacteria

Abstract

Microbial interactions driving key biogeochemical fluxes often occur within multispecies consortia that form spatially heterogeneous microenvironments. Here, we describe the “green berry” consortia of the Sippewissett salt marsh (Falmouth, MA, United States): millimeter-sized aggregates dominated by an uncultured, diazotrophic unicellular cyanobacterium of the order Chroococcales (termed GB-CYN1). We show that GB-CYN1 is closely related to Crocosphaera watsonii (UCYN-B) and “ Candidatus Atelocyanobacterium thalassa” (UCYN-A), two groups of unicellular diazotrophic cyanobacteria that play an important role in marine primary production. Other green berry consortium members include pennate diatoms and putative heterotrophic bacteria from the Alphaproteobacteria and Bacteroidetes. Tight coupling was observed between photosynthetic oxygen production and heterotrophic respiration. When illuminated, the green berries became supersaturated with oxygen. From the metagenome, we observed that GB-CYN1 encodes photosystem II genes and thus has the metabolic potential for oxygen production unlike UCYN-A. In darkness, respiratory activity rapidly depleted oxygen creating anoxia within the aggregates. Metagenomic data revealed a suite of nitrogen fixation genes encoded by GB-CYN1, and nitrogenase activity was confirmed at the whole-aggregate level by acetylene reduction assays. Metagenome reads homologous to marker genes for denitrification were observed and suggest that heterotrophic denitrifiers might co-occur in the green berries, although the physiology andmore » activity of facultative anaerobes in these aggregates remains uncharacterized. Nitrogen fixation in the surface ocean was long thought to be driven by filamentous cyanobacterial aggregates, though recent work has demonstrated the importance of unicellular diazotrophic cyanobacteria (UCYN) from the order Chroococcales. Here, the green berries serve as a useful contrast to studies of open ocean UCYN and may provide a tractable model system to investigate microbial dynamics within phytoplankton aggregates, a phenomenon of global importance to the flux of particulate organic carbon and nitrogen in surface waters.« less

Authors:
 [1];  [2];  [3];  [4];  [5];  [6];  [7]
  1. Univ. of California, Santa Barbara, CA (United States). Dept. of Ecology, Evolution, and Marine Biology
  2. Max Planck Inst. for Marine Microbiology, Bremen (Germany). HGF MPG Joint Research Group for Deep Sea Ecology and Tech.
  3. Max Planck Inst. for Marine Microbiology, Bremen (Germany). Dept. for Microbiology; Council of Norway, Oslo (Norway). Div. for Science, Research
  4. Harvard Univ., Cambridge, MA (United States). Dept. of Organismic and Evolutionary Biology
  5. Univ. of California, Davis, CA (United States). Genome Center, Dept. of Evolution and Ecology
  6. Cornell Univ., Ithaca, NY (United States). School of Integrative Plant Science
  7. Cornell Univ., Ithaca, NY (United States). Dept. of Microbiology
Publication Date:
Research Org.:
Marine Biological Lab., Woods Hole, MA (United States)
Sponsoring Org.:
USDOE
OSTI Identifier:
1468986
Grant/Contract Number:  
FG02-85ER13361
Resource Type:
Accepted Manuscript
Journal Name:
Frontiers in Microbiology
Additional Journal Information:
Journal Volume: 8; Journal ID: ISSN 1664-302X
Publisher:
Frontiers Research Foundation
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Wilbanks, Elizabeth G., Salman-Carvalho, Verena, Jaekel, Ulrike, Humphrey, Parris T., Eisen, Jonathan A., Buckley, Daniel H., and Zinder, Stephen H. The Green Berry Consortia of the Sippewissett Salt Marsh: Millimeter-Sized Aggregates of Diazotrophic Unicellular Cyanobacteria. United States: N. p., 2017. Web. doi:10.3389/fmicb.2017.01623.
Wilbanks, Elizabeth G., Salman-Carvalho, Verena, Jaekel, Ulrike, Humphrey, Parris T., Eisen, Jonathan A., Buckley, Daniel H., & Zinder, Stephen H. The Green Berry Consortia of the Sippewissett Salt Marsh: Millimeter-Sized Aggregates of Diazotrophic Unicellular Cyanobacteria. United States. doi:10.3389/fmicb.2017.01623.
Wilbanks, Elizabeth G., Salman-Carvalho, Verena, Jaekel, Ulrike, Humphrey, Parris T., Eisen, Jonathan A., Buckley, Daniel H., and Zinder, Stephen H. Mon . "The Green Berry Consortia of the Sippewissett Salt Marsh: Millimeter-Sized Aggregates of Diazotrophic Unicellular Cyanobacteria". United States. doi:10.3389/fmicb.2017.01623. https://www.osti.gov/servlets/purl/1468986.
@article{osti_1468986,
title = {The Green Berry Consortia of the Sippewissett Salt Marsh: Millimeter-Sized Aggregates of Diazotrophic Unicellular Cyanobacteria},
author = {Wilbanks, Elizabeth G. and Salman-Carvalho, Verena and Jaekel, Ulrike and Humphrey, Parris T. and Eisen, Jonathan A. and Buckley, Daniel H. and Zinder, Stephen H.},
abstractNote = {Microbial interactions driving key biogeochemical fluxes often occur within multispecies consortia that form spatially heterogeneous microenvironments. Here, we describe the “green berry” consortia of the Sippewissett salt marsh (Falmouth, MA, United States): millimeter-sized aggregates dominated by an uncultured, diazotrophic unicellular cyanobacterium of the order Chroococcales (termed GB-CYN1). We show that GB-CYN1 is closely related to Crocosphaera watsonii (UCYN-B) and “Candidatus Atelocyanobacterium thalassa” (UCYN-A), two groups of unicellular diazotrophic cyanobacteria that play an important role in marine primary production. Other green berry consortium members include pennate diatoms and putative heterotrophic bacteria from the Alphaproteobacteria and Bacteroidetes. Tight coupling was observed between photosynthetic oxygen production and heterotrophic respiration. When illuminated, the green berries became supersaturated with oxygen. From the metagenome, we observed that GB-CYN1 encodes photosystem II genes and thus has the metabolic potential for oxygen production unlike UCYN-A. In darkness, respiratory activity rapidly depleted oxygen creating anoxia within the aggregates. Metagenomic data revealed a suite of nitrogen fixation genes encoded by GB-CYN1, and nitrogenase activity was confirmed at the whole-aggregate level by acetylene reduction assays. Metagenome reads homologous to marker genes for denitrification were observed and suggest that heterotrophic denitrifiers might co-occur in the green berries, although the physiology and activity of facultative anaerobes in these aggregates remains uncharacterized. Nitrogen fixation in the surface ocean was long thought to be driven by filamentous cyanobacterial aggregates, though recent work has demonstrated the importance of unicellular diazotrophic cyanobacteria (UCYN) from the order Chroococcales. Here, the green berries serve as a useful contrast to studies of open ocean UCYN and may provide a tractable model system to investigate microbial dynamics within phytoplankton aggregates, a phenomenon of global importance to the flux of particulate organic carbon and nitrogen in surface waters.},
doi = {10.3389/fmicb.2017.01623},
journal = {Frontiers in Microbiology},
number = ,
volume = 8,
place = {United States},
year = {2017},
month = {9}
}

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