Overlooked and widespread pennate diatom-diazotroph symbioses in the sea

Christopher R Schvarcz,David M Karl,Qian Li,Angelicque E White,Grieg F Steward,Rosalina Stancheva,Mathieu Caffin,Samuel T Wilson,Jonathan P Zehr,Kendra A Turk-Kubo

doi:10.1038/s41467-022-28065-6

Abstract

Persistent nitrogen depletion in sunlit open ocean waters provides a favorable ecological niche for nitrogen-fixing (diazotrophic) cyanobacteria, some of which associate symbiotically with eukaryotic algae. All known marine examples of these symbioses have involved either centric diatom or haptophyte hosts. We report here the discovery and characterization of two distinct marine pennate diatom-diazotroph symbioses, which until now had only been observed in freshwater environments. Rhopalodiaceae diatoms Epithemia pelagica sp. nov. and Epithemia catenata sp. nov. were isolated repeatedly from the subtropical North Pacific Ocean, and analysis of sequence libraries reveals a global distribution. These symbioses likely escaped attention because the endosymbionts lack fluorescent photopigments, have nifH gene sequences similar to those of free-living unicellular cyanobacteria, and are lost in nitrogen-replete medium. Marine Rhopalodiaceae-diazotroph symbioses are a previously overlooked but widespread source of bioavailable nitrogen in marine habitats and provide new, easily cultured model organisms for the study of organelle evolution.

Highlights

Persistent nitrogen depletion in sunlit open ocean waters provides a favorable ecological niche for nitrogen-fixing cyanobacteria, some of which associate symbiotically with eukaryotic algae
We show that Epithemia symbionts are globally distributed in the marine environment and that E. pelagica and E. catenata symbioses exhibit unique daily patterns of N2 fixation
The Epithemia strains were isolated from seawater samples collected from the subtropical North Pacific Ocean at Station ALOHA (22°45' N, 158°00' W)[16]

Summary

Introduction

Persistent nitrogen depletion in sunlit open ocean waters provides a favorable ecological niche for nitrogen-fixing (diazotrophic) cyanobacteria, some of which associate symbiotically with eukaryotic algae. Pelagica symbioses indicated host LSU and EpSB nifH gene copies as high as 18 ± 8 × 103 L−1 and 0.7 ± 0.2 × 103 L−1, respectively (Supplementary Fig. 22a).

Results

Conclusion