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

Kyoko Hagino,Takeo Horiguchi,Ryo Onuma,Masanobu Kawachi,Celine Brochier-Armanet

doi:10.1371/journal.pone.0081749

Kyoko Hagino, Takeo Horiguchi + Show 3 more

Open Access

https://doi.org/10.1371/journal.pone.0081749

Copy DOI

Abstract

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.

Highlights

The family Braarudosphaeraceae are single-celled coastal phytoplanktonic algae characterized by bearing calcareous scales with five-fold symmetry, called pentaliths (Fig. 1A-C)
The phylogeny and ecology of the Braarudosphaeraceae are of considerable interest since they have a long fossil record extending back to the early Cretaceous [1], and they are one of the survivors of the K/Pg mass extinction that resulted in the demise of ca. 76% of species with fossil record [2] including ca. 90% of coccolithophores [1]
The Braarudosphaeraceae contained as many as six genera and many species, but their diversity has declined since the Eocene [3,4] and only two extant species, Braarudosphaera bigelowii (Gran & Braarud) Deflandre and B. magnei Lefort, have been described

Summary

Introduction

The family Braarudosphaeraceae are single-celled coastal phytoplanktonic algae characterized by bearing calcareous scales with five-fold symmetry, called pentaliths (Fig. 1A-C). The phylogeny and ecology of the Braarudosphaeraceae are of considerable interest since they have a long fossil record extending back to the early Cretaceous [1], and they are one of the survivors of the K/Pg mass extinction that resulted in the demise of ca. The Braarudosphaeraceae contained as many as six genera and many species, but their diversity has declined since the Eocene [3,4] and only two extant species, Braarudosphaera bigelowii (Gran & Braarud) Deflandre and B. magnei Lefort, have been described. B. bigelowii has a fossil record from the Late Cretaceous B. magnei is assigned to Braarudosphaera, its phylogenetic affinity has not been verified by either detailed morphological observations or molecular genetics

Methods

Results

Conclusion