Unique genome evolution in an intracellular N2-fixing symbiont of a rhopalodiacean diatom

Abstract

Cyanobacteria, the major photosynthetic prokaryotic lineage, are also known as a major nitrogen fixer in nature. N 2 -fixing cyanobacteria are frequently found in symbioses with various types of eukaryotes and supply fixed nitrogen compounds to their eukaryotic hosts, which congenitally lack N 2 -fixing abilities. Diatom species belonging to the family Rhopalodiaceae also possess cyanobacterial symbionts called spheroid bodies. Unlike other cyanobacterial N 2 -fixing symbionts, the spheroid bodies reside in the cytoplasm of the diatoms and are inseparable from their hosts. Recently, the first spheroid body genome from a rhopalodiacean diatom has been completely sequenced. Overall features of the genome sequence showed significant reductive genome evolution resulting in a diminution of metabolic capacity. Notably, despite its cyanobacterial origin, the spheroid body was shown to be truly incapable of photosynthesis implying that the symbiont energetically depends on the host diatom. The comparative genome analysis between the spheroid body and another N 2 -fixing symbiotic cyanobacterial group corresponding to the UCYN-A phylotypes -both were derived from cyanobacteria closely related to genus Cyanothece -revealed that the two symbionts are on similar, but explicitly distinct tracks of reductive evolution. Intimate symbiotic relationships linked by nitrogen fixation as seen in rhopalodiacean diatoms may help us better understand the evolution and mechanisms of bacterium-eukaryote endosymbioses.

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

“…Intriguingly, we found a number of endosymbiotic coccoid cyanobacterial descendants to be closely related to Crocosphaera. Endosymbionts (spheroid bodies) of rhopalodiacean diatom genera, such as Epithemia and Rhopalodia, were demonstrated to be capable of nitrogen fixation that presumably provides an advantage to the host (Nakayama et al 2011, Nakayama andInagaki 2014). Besides, these endosymbionts exhibit a morphology and even thylakoid arrangement similar to those of Crocosphaera (Bergman et al 1997).…”

Did some red alga‐derived plastids evolve via kleptoplastidy? A hypothesis

“…()]. The paradigm implies an absolute absence of protein import in the thousands of diverse endosymbionts (of both eukaryotic and prokaryotic origin) which exist in their distinct hosts (of both eukaryotic and prokaryotic origin) as permanent or temporary entities (reviewed in Bodył, Mackiewicz & Stiller, ; Stoecker et al., ; Nowack & Melkonian, ; McCutcheon & Moran, ; Keeling, ; Johnson, 2011 a,b ; Nakayama & Inagaki, ).…”

“…Thus, Cavalier-Smith & Lee (1985) provided a strict demarcation between endosymbionts and organelles, in which the unique feature (or hallmark) of organelles of endosymbiotic origin is the import of nuclear-encoded proteins [see also Cavalier-Smith (2013) and Zimorski et al (2014)]. The paradigm implies an absolute absence of protein import in the thousands of diverse endosymbionts (of both eukaryotic and prokaryotic origin) which exist in their distinct hosts (of both eukaryotic and prokaryotic origin) as permanent or temporary entities (reviewed in Bodył, Mackiewicz & Stiller, 2007;Stoecker et al, 2009;Nowack & Melkonian, 2010;McCutcheon & Moran, 2011;Keeling, 2011;Johnson, 2011a,b;Nakayama & Inagaki, 2014).…”

Letter from the Editors

“…These endosymbioses are very interesting from the perspective of the primary endosymbiosis in Archaeplastida because the first driving force for the establishment of the engulfed cyanobacterium as the permanent endosymbiont, and then the true cell organelle, could be N 2 fixation [4]. Moreover, it is possible that some of these endosymbionts with highly reduced genomes, such as the cyanobacterial UCYN-A phylotype [24], import proteins encoded by the host nucleus and thus extend the list of cell organelles.…”

“…They also identify, for the first time, the homolog of Tic62 in both Paulinella strains. In their review, Nakayama and Inagaki [24] focus on the genome evolution in the N 2 -fixing cyanobacterial endosymbionts of diatoms. These endosymbioses are very interesting from the perspective of the primary endosymbiosis in Archaeplastida because the first driving force for the establishment of the engulfed cyanobacterium as the permanent endosymbiont, and then the true cell organelle, could be N 2 fixation [4].…”