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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 and activitymore » 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. https://doi.org/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. https://doi.org/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 = {Mon Sep 04 00:00:00 EDT 2017},
month = {Mon Sep 04 00:00:00 EDT 2017}
}

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Works referenced in this record:

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journal, January 2014


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journal, February 2012

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  • Systematic Biology, Vol. 61, Issue 3
  • DOI: 10.1093/sysbio/sys029

The nitrogen-fixing gene (nifH) of Rhodopseudomonas palustris: a case of lateral gene transfer?
journal, July 2004


Bacterial Associations with Marine Oscillatoria sp. (Trichodesmium sp.) Populations: Ecophysiological Implications1
journal, December 1989


Characterization of diatom–cyanobacteria symbioses on the basis of nifH, hetR and 16S rRNA sequences
journal, November 2006


Phenotypic and genotypic characterization of multiple strains of the diazotrophic cyanobacterium, Crocosphaera watsonii , isolated from the open ocean
journal, February 2009


Physiology of purple sulfur bacteria forming macroscopic aggregates in Great Sippewissett Salt Marsh, Massachusetts
journal, August 1993


Complexity of cyanobacterial exopolysaccharides: composition, structures, inducing factors and putative genes involved in their biosynthesis and assembly
journal, September 2009


Whole genome comparison of six Crocosphaera watsonii strains with differing phenotypes
journal, July 2013

  • Bench, Shellie R.; Heller, Philip; Frank, Ildiko
  • Journal of Phycology, Vol. 49, Issue 4
  • DOI: 10.1111/jpy.12090

Globally Distributed Uncultivated Oceanic N2-Fixing Cyanobacteria Lack Oxygenic Photosystem II
journal, November 2008


Unicellular Cyanobacterium Symbiotic with a Single-Celled Eukaryotic Alga
journal, September 2012


Direct Measurement of O2-Depleted Microzones in Marine Oscillatoria: Relation to N2 Fixation
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Unicellular, aerobic nitrogen-fixing cyanobacteria of the genus Cyanothece.
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The metagenomics RAST server – a public resource for the automatic phylogenetic and functional analysis of metagenomes
journal, September 2008


Accelerated Profile HMM Searches
journal, October 2011


FastTree 2 – Approximately Maximum-Likelihood Trees for Large Alignments
journal, March 2010


Community Structure and Functional Gene Profile of Bacteria on Healthy and Diseased Thalli of the Red Seaweed Delisea pulchra
journal, December 2012


Discovery of an Endosymbiotic Nitrogen-Fixing Cyanobacterium UCYN-A in Braarudosphaera bigelowii (Prymnesiophyceae)
journal, December 2013


Anoxic aggregates - an ephemeral phenomenon in the pelagic environment?
journal, January 1997

  • Ploug, H.; Kühl, M.; Buchholz-Cleven, B.
  • Aquatic Microbial Ecology, Vol. 13
  • DOI: 10.3354/ame013285

Evidence and a conceptual model for the co‑occurrence of nitrogen fixation and denitrification in heterotrophic marine sediments
journal, May 2013

  • Fulweiler, Rw; Brown, Sm; Nixon, Sw
  • Marine Ecology Progress Series, Vol. 482
  • DOI: 10.3354/meps10240

No sign of denitrification in a Baltic Sea cyanobacterial bloom
journal, January 2002

  • Hietanen, S.; Moisander, Ph; Kuparinen, J.
  • Marine Ecology Progress Series, Vol. 242
  • DOI: 10.3354/meps242073

Photosynthetic characteristics of Trichodesmium in the southwest Pacific Ocean: importance and significance
journal, May 2007

  • Masotti, I.; Ruiz-Pino, D.; Le Bouteiller, A.
  • Marine Ecology Progress Series, Vol. 338
  • DOI: 10.3354/meps338047

Constitutive Extracellular Polysaccharide (EPS) Production by Specific Isolates of Crocosphaera watsonii
journal, January 2011


Two Strains of Crocosphaera watsonii with Highly Conserved Genomes are Distinguished by Strain-Specific Features
journal, January 2011

  • Bench, Shellie R.; Ilikchyan, Irina N.; Tripp, H. James
  • Frontiers in Microbiology, Vol. 2
  • DOI: 10.3389/fmicb.2011.00261

Nitrogen fixation by algae in a Massachusetts salt marsh 1: N
journal, March 1978

  • Carpenter, Edward J.; Van Raalte, Charlene D.; Valiela, Ivan
  • Limnology and Oceanography, Vol. 23, Issue 2
  • DOI: 10.4319/lo.1978.23.2.0318

Primary production of microalgae in sediments measured by oxygen microprofile, H 14 CO 3 - fixation, and oxygen exchange methods1 : Primary production of sediments
journal, July 1981

  • Revsbech, Niels Peter; JØrgensen, Bo Barker; Brix, Ole
  • Limnology and Oceanography, Vol. 26, Issue 4
  • DOI: 10.4319/lo.1981.26.4.0717

Nitrogen fixation in freshwater, estuarine, and marine ecosystems. 1. Rates and importance
journal, January 1988


Phylogenetic diversity of aggregate-attached vs. free-living marine bacterial assemblages
journal, July 1993

  • DeLong, Edward F.; Franks, Diana G.; Alldredge, Alice L.
  • Limnology and Oceanography, Vol. 38, Issue 5
  • DOI: 10.4319/lo.1993.38.5.0924

Direct measurement of diffusivity within diatom aggregates containing transparent exopolymer particles
journal, January 2007


Experiments linking nitrogenase gene expression to nitrogen fixation in the North Pacific subtropical gyre
journal, January 2007

  • Zehr, Jonathan P.; Montoya, Joseph P.; Jenkins, Bethany D.
  • Limnology and Oceanography, Vol. 52, Issue 1
  • DOI: 10.4319/lo.2007.52.1.0169

Influence of the Amazon River plume on distributions of free-living and symbiotic cyanobacteria in the western tropical north Atlantic Ocean
journal, March 2007


Works referencing / citing this record:

Diverse diazotrophs are present on sinking particles in the North Pacific Subtropical Gyre
journal, August 2018


Diverse diazotrophs are present on sinking particles in the North Pacific Subtropical Gyre
journal, August 2018