Complete genome of a nonphotosynthetic cyanobacterium in a diatom reveals recent adaptations to an intracellular lifestyle

Abstract

The evolution of mitochondria and plastids from bacterial endosymbionts were key events in the origin and diversification of eukaryotic cells. Although the ancient nature of these organelles makes it difficult to understand the earliest events that led to their establishment, the study of eukaryotic cells with recently evolved obligate endosymbiotic bacteria has the potential to provide important insight into the transformation of endosymbionts into organelles. Diatoms belonging to the family Rhopalodiaceae and their endosymbionts of cyanobacterial origin (i.e., "spheroid bodies") are emerging as a useful model system in this regard. The spheroid bodies, which appear to enable rhopalodiacean diatoms to use gaseous nitrogen, became established after the divergence of extant diatom families. Here we report what is, to our knowledge, the first complete genome sequence of a spheroid body, that of the rhopalodiacean diatom Epithemia turgida. The E. turgida spheroid body (EtSB) genome was found to possess a gene set for nitrogen fixation, as anticipated, but is reduced in size and gene repertoire compared with the genomes of their closest known free-living relatives. The presence of numerous pseudogenes in the EtSB genome suggests that genome reduction is ongoing. Most strikingly, our genomic data convincingly show that the EtSB has lost photosynthetic ability and is metabolically dependent on its host cell, unprecedented characteristics among cyanobacteria, and cyanobacterial symbionts. The diatom-spheroid body endosymbiosis is thus a unique system for investigating the processes underlying the integration of a bacterial endosymbiont into eukaryotic cells.photosynthesis | organelle evolution | pseudogenization

Diversification of DnaA dependency for DNA replication in cyanobacterial evolution

“…Thus, the evolutionary history of DNA replication from a cyanobacterial to a plastid system can be discerned from genetic evidence. Interestingly, dnaA is the only gene that is not conserved between red algae, the cyanobacterial symbiont Diversification of cyanobacterial DNA replication R Ohbayashi et al Nostoc azollae (Ran et al, 2010) and the spheroid bodies (Nakayama et al, 2014) of diatoms. We have shown that cyanobacteria have the capacity to shift the DNA replication initiation system from chromosomal to plasmid type by dnaA deletion.…”

“…As such, DnaA is essential for DNA replication initiation in most bacteria. Indeed, with the exception of certain symbiotic species, there are no known free-living, DnaA-independent bacteria (Akman et al, 2002;Ran et al, 2010;Nakayama et al, 2014).…”

Paulinella chromatophora – rethinking the transition from endosymbiont to organelle

“…There are other examples of highly reduced cyanobacterial endosymbionts, such as Candidatus Atelocyanobacterium thalassa living symbiotically with a haptophyte alga [85] or the "spheroid bodies" in rhopalodiacean diatoms [86,87]. However, these symbionts lost their ability to perform oxygenic photosynthesis and their main function is thought to be nitrogen fixation.…”

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

“…However, only a handful of molecular studies have been done on the spheroid bodies and their host diatoms to date, and the biological, evolutionary, and/or environmental backgrounds, which facilitated this unique symbiosis, remain uncertain. Recently our research group successfully determined the first whole genome sequence of a spheroid body in the rhopalodiacean diatom Epithemia turgida [14]. The detailed metabolic functions deduced from the spheroid body genome indicated that the cyanobacterial symbionts reduced its metabolic capacity including photosynthesis, suggesting that the symbiont has abandoned a photoautotrophic lifestyle and energetically depends on its host.…”

“…Against this background, we determined a complete genome sequence of the spheroid body in the rhopalodiacean diatom E. turgida [14]. A 16S rDNA phylogenetic tree of the symbionts indicated that the spheroid bodies of genera Rhopalodia and Epithemia have a single origin, implying that the spheroid bodies diverged along with the speciation of rhopalodiacean diatoms [5].…”