Unstable Relationship Between Braarudosphaera bigelowii (= Chrysochromulina parkeae) and Its Nitrogen-Fixing Endosymbiont.

Shigekatsu Suzuki,Kyoko Hagino,Masanobu Kawachi,Atsushi Nakamura,Chinatsu Tsukakoshi,Ken-Ichiro Ishida,Isao Inouye

doi:10.3389/fpls.2021.749895

Abstract

Marine phytoplankton are major primary producers, and their growth is primarily limited by nitrogen in the oligotrophic ocean environment. The haptophyte Braarudosphaera bigelowii possesses a cyanobacterial endosymbiont (UCYN-A), which plays a major role in nitrogen fixation in the ocean. However, host-symbiont interactions are poorly understood because B. bigelowii was unculturable. In this study, we sequenced the complete genome of the B. bigelowii endosymbiont and showed that it was highly reductive and closely related to UCYN-A2 (an ecotype of UCYN-A). We succeeded in establishing B. bigelowii strains and performed microscopic observations. The detailed observations showed that the cyanobacterial endosymbiont was surrounded by a single host derived membrane and divided synchronously with the host cell division. The transcriptome of B. bigelowii revealed that B. bigelowii lacked the expression of many essential genes associated with the uptake of most nitrogen compounds, except ammonia. During cultivation, some of the strains completely lost the endosymbiont. Moreover, we did not find any evidence of endosymbiotic gene transfer from the endosymbiont to the host. These findings illustrate an unstable morphological, metabolic, and genetic relationship between B. bigelowii and its endosymbiont.

Highlights

Marine phytoplankton consume various nitrogen compounds, such as nitrate, nitrite, ammonia, and cyanate, and often produce large-scale blooms triggered by the abundance of specific nitrogen compounds (Suzuki et al, 2019)
The complete genome of the ecotype UCYN-A1 was sequenced by whole-genome amplification (WGA) of cells purified by flow cytometry (Zehr et al, 2008; Tripp et al, 2010)
Cells were covered with multi-layered oval scales of three types and 3–6 long spinelike scales at the anterior and posterior ends (Figures 1A–D; Supplementary Figures 1, 2). These morphological features were consistent with the original description of C. parkeae (Green and Leadbeater, 1972), synonymous with B. bigelowii (Hagino et al, 2013); we identified these strains

Summary

INTRODUCTION

Marine phytoplankton consume various nitrogen compounds, such as nitrate, nitrite, ammonia, and cyanate, and often produce large-scale blooms triggered by the abundance of specific nitrogen compounds (Suzuki et al, 2019). The complete genome of the ecotype UCYN-A1 was sequenced by whole-genome amplification (WGA) of cells purified by flow cytometry (Zehr et al, 2008; Tripp et al, 2010). The draft genome of UCYN-A2 was sequenced using a similar WGA method (i.e., using cells isolated by flow cytometry; Bombar et al, 2014). Braarudosphaera bigelowii is a species complex consisting of multiple pseudo-cryptic species based on genetic and morphological divergence (Hagino et al, 2009). In this species complex, 18S rDNA genotype III is considered B. bigelowii sensu stricto (s.s.). Transcriptome analyses were performed to elucidate nitrogen metabolism in B. bigelowii

MATERIALS AND METHODS

RESULTS AND DISCUSSION

DATA AVAILABILITY STATEMENT