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

Braarudosphaera bigelowii (Prymnesiophyceae) is a coastal coccolithophore with a long fossil record, extending back to the late Cretaceous (ca. 100 Ma). A recent study revealed close phylogenetic relationships between B. bigelowii, Chrysochromulina parkeae (Prymnesiophyceae), and a prymnesiophyte that forms a symbiotic association with the nitrogen-fixing cyanobacterium UCYN-A. In order to further examine these relationships, we conducted transmission electron microscopic and molecular phylogenetic studies of B. bigelowii. TEM studies showed that, in addition to organelles, such as the nucleus, chloroplasts and mitochondria, B. bigelowii contains one or two spheroid bodies with internal lamellae. In the 18S rDNA tree of the Prymnesiophyceae, C. parkeae fell within the B. bigelowii clade, and was close to B. bigelowii Genotype III (99.89% similarity). Plastid 16S rDNA sequences obtained from B. bigelowii were close to the unidentified sequences from the oligotrophic SE Pacific Ocean (e.g. HM133411) (99.86% similarity). Bacterial16S rDNA sequences obtained from B. bigelowii were identical to the UCYN-A sequence AY621693 from Arabian Sea, and fell in the UCYN-A clade. From these results, we suggest that; 1) C. parkeae is the alternate life cycle stage of B. bigelowii sensu stricto or that of a sibling species of B. bigelowii, and 2) the spheroid body of B. bigelowii originated from endosymbiosis of the nitrogen-fixing cyanobacterium UCYN-A.

• Publication year

  2013

• Venue

  PLoS ONE

• Publication date

  2013-12-04

• Fields of study

  Biology, Medicine, Environmental Science

• Identifiers
  DOI 10.1371/journal.pone.0081749PMID 24324722PMCID 3852252
• External record

  Open on Semantic Scholar

• Source metadata

  Semantic Scholar, PubMed

• No claims are published for this paper.

• No concepts are published for this paper.

• In situ identification and N₂ and C fixation rates of uncultivated cyanobacteria populations.

  2013cited by this paper
• Ultrastructural and molecular characterization of cyanobacterial symbionts in Dictyocoryne profunda (polycystine radiolaria)

  2012cited by this paper
• Unicellular Cyanobacterium Symbiotic with a Single-Celled Eukaryotic Alga

  2012influential reference
• Isolation and characterization of the unicellular diazotrophic cyanobacterium Group C TW3 from the tropical western Pacific Ocean.

  2012cited by this paper
• Body Mass Index and Diabetes in Asia: A Cross-Sectional Pooled Analysis of 900,000 Individuals in the Asia Cohort Consortium

  2011cited by this paper
• Plastid 16S rRNA Gene Diversity among Eukaryotic Picophytoplankton Sorted by Flow Cytometry from the South Pacific Ocean

  2011influential reference
• Ribosomal DNA phylogenies and a morphological revision provide the basis for a revised taxonomy of the Prymnesiales (Haptophyta)

  2011influential reference
• Pseudo-cryptic speciation in Braarudosphaera bigelowii (Gran and Braarud) Deflandre

  2009influential reference
• Groups without Cultured Representatives Dominate Eukaryotic Picophytoplankton in the Oligotrophic South East Pacific Ocean

  2009influential reference
• Critical Role of Arcuate Y4 Receptors and the Melanocortin System in Pancreatic Polypeptide-Induced Reduction in Food Intake in Mice

  2009cited by this paper
• Chrysochromulina palpebralis sp. nov. (Prymnesiophyceae): a haptophyte, possessing two alternative morphologies

  2009cited by this paper
• A molecular clock for coccolithophores and implications for selectivity of phytoplankton extinctions across the K/T boundary

  2008cited by this paper
• Globally Distributed Uncultivated Oceanic N2-Fixing Cyanobacteria Lack Oxygenic Photosystem II

  2008cited by this paper
• LIGHT AND ELECTRON MICROSCOPE OBSERVATIONS OF ALGIROSPHAERA ROBUSTA (PRYMNESIOPHYCEAE) 1

  2007cited by this paper
• Living Braarudosphaera bigelowii (Gran & Braarud) Deflandre in the Bering Sea.

  2007cited by this paper
• UNICELLULAR CYANOBIONTS IN OPEN OCEAN DINOFLAGELLATES, RADIOLARIANS, AND TINTINNIDS: ULTRASTRUCTURAL CHARACTERIZATION AND IMMUNO‐LOCALIZATION OF PHYCOERYTHRIN AND NITROGENASE 1

  2006cited by this paper
• Phylogenetic affinities of an enigmatic nannoplankton, Braarudosphaera bigelowii based on the SSU rDNA sequences

  2006influential reference
• Coccolithophore assemblages and morphotypes of Emiliania huxleyi in the boundary zone between the cold Oyashio and warm Kuroshio currents off the coast of Japan

  2005cited by this paper
• Selective calcareous nannoplankton survivorship at the Cretaceous-Tertiary boundary

  2005cited by this paper
• Coccolithophores: From Molecular Processes to Global Impact

  2005cited by this paper
• PCR Analysis of the Distribution of Unicellular Cyanobacterial Diazotrophs in the Arabian Sea

  2004cited by this paper
• Surface ultrastructure and molecular phylogenetics of four unarmored heterotrophic dinoflagellates, including the type species of the genus Gyrodinium (Dinophyceae)

  2004influential reference
• Calcareous nannoplankton evolution and diversity through time

  2004cited by this paper
• MrModeltest 2.2. Program Distributed by the Author

  2004cited by this paper
• Intracellular spheroid bodies of Rhopalodia gibba have nitrogen-fixing apparatus of cyanobacterial origin.

  2004cited by this paper
• MrBayes 3: Bayesian phylogenetic inference under mixed models

  2003cited by this paper
• A guide to extant coccolithophore taxonomy.

  2003influential reference
• PAUP*: Phylogenetic analysis using parsimony (*and other methods), Version 4.0b10

  2002cited by this paper
• Unicellular cyanobacteria fix N2 in the subtropical North Pacific Ocean

  2001cited by this paper
• New examples of holococcolith¯heterococcolith combination coccospheres and their implications for coccolithophorid biology.

  2000cited by this paper
• PAUP* Phylogenetic analysis using parsimony (*and other methods) Version 4

  2000cited by this paper
• Unusual Oligocene Braarudosphaera-rich layers of the South Atlantic and their palaeoceanograpghic implications.

  1999cited by this paper
• Quantifying Microbial Diversity: Morphotypes, 16S rRNA Genes, and Carotenoids of Oxygenic Phototrophs in Microbial Mats

  1999cited by this paper
• Coccolith ultrastructure and biomineralisation

  1999cited by this paper
• MODELTEST: testing the model of DNA substitution

  1998cited by this paper
• Fossil Coccospheres from the K/T Boundary Section from Geulhemmerberg, the Netherlands

  1997cited by this paper
• The life-cycle of Emiliania huxleyi: A brief review and a study of relative ploidy levels analysed by flow cytometry

  1996cited by this paper
• The phylogenetic relationship between the Chlamydomonadales and Chlorococcales inferred from 18SrDNA sequence data

  1996influential reference
• Extinctions in the fossil record

  1994cited by this paper
• Calcareous Nannoplankton Thanatocoenoses in Surface Sediments from Seas Around Japan

  1991cited by this paper
• 16S/23S rRNA sequencing

  1991cited by this paper
• CONFIDENCE LIMITS ON PHYLOGENIES: AN APPROACH USING THE BOOTSTRAP

  1985cited by this paper
• New observations on the Coccolithophorid Umbilicosphaera sibogae var. foliosa (Prymnesiophyceae) with reference to cell covering, cell structure and flagellar apparatus

  1984cited by this paper
• The taxonomy of Prymnesium (Prymnesiophyceae) including a description of a new cosmopolitan species, P. Patellifera sp. nov., and further observations on P. parvum N. carter

  1982cited by this paper
• Chrysochromulina Parkeae Sp.Nov. [Haptophyceae] a New Species Recorded From S.W. England and Norway

  1972cited by this paper
• 605. A NOTE ON THE DISTRIBUTION OF BRAARUDOSPHAERA BIGELOWI (GRAN AND BRAARUD) DEFLANDRE IN THE BOTTOM SEDIMENTS OF SENDAI BAY, JAPAN

  1972cited by this paper
• Coccolithus huxleyi (Lohm.) Kamptn II. The flagellate cell, aberrant cell types, vegetative propagation and life cycles

  1972cited by this paper
• Fine structure of an unusual cytoplasmic inclusion in the diatom genus,Rhopalodia

  1965cited by this paper
• The motile (Crystallolithus hyalinus Gaarder & Markali) and non-motile phases in the life history of Coccolithus pelagicus (Wallich) Schiller

  1960cited by this paper

• Spatiotemporal heterogeneity in diazotrophic communities reveals novel niche zonation on the continental shelf of the East China Sea

  2026cites this paper
• Impact of diazotrophs on marine food webs and the biological carbon pump: progress and remaining challenges

  2026cites this paper
• Genomes of N2-fixing endosymbionts of unicellular eukaryotes and host-independence

  2026cites this paper
• Redefining the nitroplast: Recent insights into the endosymbiont-to-organelle transition

  2025cites this paper
• Picophytoplankton implicated in productivity and biogeochemistry in the North Pacific Transition Zone

  2025cites this paper
• Design, structures, and applications of an icosahedral artificial protein nanocage, TIP60.

  2025cites this paper
• Composition, growth, succession, and function in the Cladophora microbiome: insights from quantitative Stable Isotope Probing and NanoSIMS imaging

  2025cites this paper
• Temperature‐dependent growth and activity in a globally distributed nitrogen‐fixing haptophyte

  2025cites this paper
• Biomineralization in the Calcareous Nannoplankton Phenotypic Expressions Across Life Cycles, Geometric Control on Diversification, and Origin

  2025cites this paper
• Puzzling out the ecological niche construction for nitrogen fixers in a coastal upwelling system

  2025cites this paper
• Investigation of the Cyanothece nitrogenase cluster in Synechocystis: a blueprint for engineering nitrogen-fixing photoautotrophs

  2025cites this paper
• The protist community of the oligotrophic waters of the Gulf of Mexico is distinctly shaped by depth-specific physicochemical conditions during the warm season

  2025cites this paper
• Eukaryogenesis From FECA to LECA: Radical Steps Along the Way

  2025cites this paper
• Comparative Genomics Insights Into the Evolutionary Disparities Between Nitroplast‐Evolved Ecotype UCYN‐A2 and Its Closest Relative UCYN‐A1

  2025cites this paper
• Cyclic electron flow and Photosystem II-less photosynthesis.

  2024cites this paper
• Metagenomics reveals the genetic diversity between sublineages of UCYN-A and their algal host plastids

  2024influential citation
• Protein import into bacterial endosymbionts and evolving organelles

  2024cites this paper
• Plankton food web structure and productivity under ocean alkalinity enhancement

  2024cites this paper
• Phagotrophy in the nitrogen‐fixing haptophyte Braarudosphaera bigelowii

  2024influential citation
• Changes in diazotrophic community structure associated with Kuroshio succession in the northern South China Sea

  2024cites this paper
• The endosymbiont of Epithemia clementina is specialized for nitrogen fixation within a photosynthetic eukaryote

  2024cites this paper
• Nitrogen-fixing organelle in a marine alga

  2024cites this paper
• Crocosphaera watsonii – A widespread nitrogen‐fixing unicellular marine cyanobacterium

  2024cites this paper
• Metabolic trade-offs constrain the cell size ratio in a nitrogen-fixing symbiosis.

  2024cites this paper
• Distribution of the N2 ‐fixing cyanobacterium Candidatus Atelocyanobacterium thalassa in the Mexican Pacific upwelling system under two contrasting El Niño Southern Oscillation conditions

  2024cites this paper
• The endosymbiont of Epithemia clementina is specialized for nitrogen fixation within a photosynthetic eukaryote

  2023cites this paper
• Transition from free-living cyanobacterium to endosymbiont enables adaptations favoring nitrogen fixation in a photosynthetic eukaryote.

  2023cites this paper
• Microevolutionary patterns in ecotypes of the symbiotic cyanobacterium UCYN-A revealed from a Northwest Atlantic coastal time series

  2023cites this paper
• Change in diazotrophic community structure associated with Kuroshio succession in the northern South China Sea

  2023cites this paper
• Global oceanic diazotroph database version 2 and elevated estimate of global oceanic N2 fixation

  2023cites this paper
• Molecular phylogenetic affinity of Hayaster cf . perplexus based on 18S rDNA sequences.

  2023cites this paper
• Soft X-ray Tomography Enables New Insights into the Coordinated Division of Organelle-like Symbiont in a Globally Distributed Unicellular Marine Haptophyte Alga.

  2023cites this paper
• Microalgal and Nitrogen-Fixing Bacterial Consortia: From Interaction to Biotechnological Potential

  2023cites this paper
• Nitrogen cycling during the Mesoproterozoic as informed by the 1400 million year old Xiamaling Formation

  2023cites this paper
• Culture-Independent Single-Cell PacBio Sequencing Reveals Epibiotic Variovorax and Nucleus Associated Mycoplasma in the Microbiome of the Marine Benthic Protist Geleia sp. YT (Ciliophora, Karyorelictea)

  2023cites this paper
• Symbiotic UCYN-A strains co-occurred with El Niño, relaxed upwelling, and varied eukaryotes over 10 years off Southern California

  2023cites this paper
• Quantification of gene copy numbers is valuable in marine microbial ecology: A comment to Meiler et al. (2022)

  2023cites this paper
• Seasonal and spatial patterns in diazotroph community composition at Station ALOHA

  2023cites this paper
• Primer design for the amplification of the ammonium transporter genes from the uncultured haptophyte algal species symbiotic with the marine nitrogen-fixing cyanobacterium UCYN-A1

  2023influential citation
• Open ocean and coastal strains of the N2-fixing cyanobacterium UCYN-A have distinct transcriptomes

  2022influential citation
• Crocosphaera as a Major Consumer of Fixed Nitrogen

  2022cites this paper
• Coastal upwelling enhances abundance of a symbiotic diazotroph (UCYN-A) and its haptophyte host in the Arctic Ocean

  2022cites this paper
• Interannual Variation in Phytoplankton Community Driven by Environmental Factors in the Northern East China Sea

  2022cites this paper
• Elucidation of trophic interactions in an unusual single-cell nitrogen-fixing symbiosis using metabolic modeling

  2021cites this paper
• Symbioses of Cyanobacteria in Marine Environments: Ecological Insights and Biotechnological Perspectives

  2021cites this paper
• Crocosphaera as a major consumer of fixed nitrogen despite its capability of nitrogen fixation

  2021cites this paper
• Investigating the microbial ecology of coastal hotspots of marine nitrogen fixation in the western North Atlantic

  2021cites this paper
• Unstable Relationship Between Braarudosphaera bigelowii (= Chrysochromulina parkeae) and Its Nitrogen-Fixing Endosymbiont

  2021cites this paper
• Atmospheric Deposition Promotes Relative Abundances of High‐Dimethylsulfoniopropionate Producers in the Western North Pacific

  2021cites this paper
• Size and shape variation in the calcareous nannoplankton genus Braarudosphaera following the Cretaceous/Paleogene (K/Pg) mass extinction: clues as to its evolutionary success

  2021cites this paper
• Critical Role of Light in the Growth and Activity of the Marine N2-Fixing UCYN-A Symbiosis

  2021cites this paper
• Unexpected presence of the nitrogen‐fixing symbiotic cyanobacterium UCYN‐A in Monterey Bay, California

  2020cites this paper
• Spatial variation of abundant picoeukaryotes in the subtropical Kuroshio Current in winter

  2020cites this paper
• Changing perspectives in marine nitrogen fixation

  2020cites this paper
• Global distribution patterns of marine nitrogen-fixers by imaging and molecular methods

  2020cites this paper
• Algal plankton turn to hunting to survive and recover from end-Cretaceous impact darkness

  2020cites this paper
• Diversity of potential producers of bioactive metabolites having polyketide nature in the Baikal sponge community of Rezinkovia echinata

  2020cites this paper
• Cell sorting reveals few novel prokaryote and photosynthetic picoeukaryote associations in the oligotrophic ocean

  2020cites this paper
• Quantitative models of nitrogen-fixing organisms

  2020cites this paper
• Taxonomic resolution of the genus Cyanothece (Chroococcales, Cyanobacteria), with a treatment on Gloeothece and three new genera, Crocosphaera, Rippkaea, and Zehria

  2019cites this paper
• The genetic diversity and evolution of diatom-diazotroph associations highlights traits favoring symbiont integration

  2019cites this paper
• Modeling of atomic-molecular structures by contiguous filling of space with Frank-Kasper atomic domains.

  2019cites this paper
• Correction: Filling gaps in bacterial amino acid biosynthesis pathways with high-throughput genetics

  2019cites this paper
• Phylogenetic Evidence for the Endosymbiotic Origin of Organelles

  2019cites this paper
• Transcriptome reconstruction and functional analysis of eukaryotic marine plankton communities via high-throughput metagenomics and metatranscriptomics

  2019cites this paper
• Unicellular Cyanobacteria Are Important Components of Phytoplankton Communities in Australia’s Northern Oceanic Ecoregions

  2019cites this paper
• Genomic and morphological diversity of marine planktonic diatom-diazotroph associations : a continuum of integration and diversification through geological time

  2019cites this paper
• Diversity, Genomics, and Distribution of Phytoplankton-Cyanobacterium Single-Cell Symbiotic Associations.

  2019cites this paper
• The fossil record of coastal coccolithophores.

  2019cites this paper
• Single-cell genomics unveiled a cryptic cyanobacterial lineage with a worldwide distribution hidden by a dinoflagellate host

  2019cites this paper
• Spatial Variations in Community Structure of Haptophytes Across the Kuroshio Front in the Tokara Strait

  2019cites this paper
• Phytoplankton, Calcareous Nanoplankton—The Coccolithophores

  2019cites this paper
• Late Cretaceous paleobiogeography of Braarudosphaera bigelowii

  2019cites this paper
• Transportation of Diazotroph Community From the Upstream to Downstream of the Kuroshio

  2019cites this paper
• Temporal variability of diazotroph community composition in the upwelling region off NW Iberia

  2019cites this paper
• Orbitally Forced Hyperstratification of the Oligocene South Atlantic Ocean

  2018cites this paper
• Coccolith arrangement follows Eulerian mathematics in the coccolithophore Emiliania huxleyi

  2018cites this paper
• Small eukaryotic phytoplankton communities in tropical waters off Brazil are dominated by symbioses between Haptophyta and nitrogen-fixing cyanobacteria

  2018cites this paper
• “Pomacytosis”—Semi-extracellular phagocytosis of cyanobacteria by the smallest marine algae

  2018influential citation
• A Short Comparison of Two Marine Planktonic Diazotrophic Symbioses Highlights an Un-quantified Disparity

  2018cites this paper
• Contrasting biogeography and diversity patterns between diatoms and haptophytes in the central Pacific Ocean

  2018cites this paper
• Geometry of Braarudosphaera bigelowii (Prymnesiophyceae) nannoliths

  2018cites this paper
• How did cyanobacteria first embark on the path to becoming plastids?: lessons from protist symbioses.

  2018cites this paper
• The structure of a normal, complete Emiliania huxleyi coccolith includes two oval-

  2018cites this paper
• Dynamics and interactions of highly resolved marine plankton via automated high-frequency sampling

  2017cites this paper
• Genomic divergence within non-photosynthetic cyanobacterial endosymbionts in rhopalodiacean diatoms

  2017cites this paper
• Vers la reprogrammation métabolique de la cyanobactérie modèle Synechocystis pour la production durable de biocarburants : structuration des flux du carbone par CP12 et implications sur l’équilibre bioénergétique, l’hydrogénase et l’intégrité génomique

  2017cites this paper
• Diversity, ecology and evolution of marine diazotrophic microorganisms

  2017cites this paper
• Biology of Haptophytes: Complicated Cellular Processes Driving the Global Carbon Cycle

  2017cites this paper
• Title : Re-discovery of living fossil coccolithophores from coastal water of Japan and of Croatia

  2017influential citation
• The Green Berry Consortia of the Sippewissett Salt Marsh: Millimeter-Sized Aggregates of Diazotrophic Unicellular Cyanobacteria

  2017cites this paper
• Highly heterogeneous diazotroph communities in the Kuroshio Current and the Tokara Strait, Japan

  2017cites this paper
• Contrasting seasonal drivers of virus abundance and production in the North Pacific Ocean

  2017cites this paper
• Filling gaps in bacterial amino acid biosynthesis pathways with high-throughput genetics

  2017cites this paper
• Phototrophic Microorganisms: The Basis of the Marine Food Web

  2016cites this paper
• Baltic Sea coccolithophores – an overview of insights into their taxonomy and ecology from the last 40 years.

  2016cites this paper
• Spatial and temporal variability of unicellular diazotrophic cyanobacteria in the eastern Seto Inland Sea

  2016influential citation
• New insights into the ecology of the globally significant uncultured nitrogen-fixing symbiont UCYN-A

  2016influential citation
• Photosymbiosis in Marine Pelagic Environments

  2016cites this paper
• Dynamic changes in the composition of photosynthetic picoeukaryotes in the northwestern Pacific Ocean revealed by high-throughput tag sequencing of plastid 16S rRNA genes.

  2016cites this paper