Molecular investigation of the ciliate Spirostomum semivirescens, with first transcriptome and new geographical records

Hunter N. Hines1,3*, Henning Onsbring2*, Thijs J. G. Ettema2 The ciliate Spirostomum semivirescens is a large freshwater protist densely packed with endosymbiotic algae and capable of building a protective coating from surrounding particles. The species has been rarely recorded and it lacks any molecular investigations. We obtained such data from S. semivirescens isolated in the UK and Sweden. Using single-cell RNA sequencing of isolates from both countries, the transcriptome of S. semivirescens was generated. Phylogenetic analysis of the rRNA gene cluster revealed both isolates to be identical. Additionally, rRNA sequence analysis of the green algal endosymbiont revealed that it is closely related to Chlorella vulgaris. Along with the molecular species identification, an analysis of the ciliates’ stop codons was carried out, which revealed a relationship where TGA stop codon frequency decreased with increasing gene expression levels. The observed codon bias suggests that S. semivirescens could be in an early stage of reassigning the TGA stop codon. Analysis of the transcriptome indicates that S. semivirescens potentially uses rhodoquinol-dependent fumarate reduction to respire in the oxygen-depleted habitats where it lives. The data also shows that despite large geographical distances (over 1,600 km) between the sampling sites investigated, a morphologically-identical species can share an exact molecular signature, suggesting that some ciliate species, even those over 1mm in size, could have a global biogeographical distribution

From archaeon to eukaryote : The evolutionary dark ages of the eukaryotic cell

The evolutionary origin of the eukaryotic cell represents an enigmatic, yet largely incomplete, puzzle. Several mutually incompatible scenarios have been proposed to explain how the eukaryotic domain of life could have emerged. To date, convincing evidence for these scenarios in the form of intermediate stages of the proposed eukaryogenesis trajectories is lacking, presenting the emergence of the complex features of the eukaryotic cell as an evolutionary deus ex machina. However, recent advances in the field of phylogenomics have started to lend support for a model that places a cellular fusion event at the basis of the origin of eukaryotes (symbiogenesis), involving the merger of an as yet unknown archaeal lineage that most probably belongs to the recently proposed 'TACK superphylum' (comprising Thaumarchaeota, Aigarchaeota, Crenarchaeota and Korarchaeota) with an alphaproteobacterium (the protomitochondrion). Interestingly, an increasing number of so-called ESPs (eukaryotic signature proteins) is being discovered in recently sequenced archaeal genomes, indicating that the archaeal ancestor of the eukaryotic cell might have been more eukaryotic in nature than presumed previously, and might, for example, have comprised primitive phagocytotic capabilities. In the present paper, we review the evolutionary transition from archaeon to eukaryote, and propose a new model for the emergence of the eukaryotic cell, the 'PhAT (phagocytosing archaeon theory)', which explains the emergence of the cellular and genomic features of eukaryotes in the light of a transiently complex phagocytosing archaeon.</p

The symbiosis that changed the world

All cellular life on Earth can be classified into one of the three domains: bacteria, archaea or eukaryotes. Whereas cells of bacteria and archaea are small and simple, those of eukaryotes are generally bigger and complex, containing a nucleus that encompasses DNA, and other subcellular compartments, referred to as organelles

FtsZ-less cell division in archaea and bacteria

A dedicated cell division machinery is needed for efficient proliferation of an organism. The eukaryotic actin-myosin based mechanism and the bacterial FtsZ-dependent machinery have both been characterized in detail, and a third division mechanism, the Cdv system, was recently discovered in archaea from the Crenarchaeota phylum. Despite these findings, division mechanisms remain to be identified in, for example, organisms belonging to the bacterial PVC superphylum, bacteria with extremely reduced genomes, wall-less archaea and bacteria, and in archaea that carry out the division process without cell constriction. Cytokinesis mechanisms in these clades and individual taxa are likely to include adaptation of host functions to division of bacterial symbionts, transfer of bacterial division genes into the host genome, vesicle formation without a dedicated constriction machinery, cross-wall formation without invagination, as well as entirely novel division mechanisms.</p

The symbiosis that changed the world

All cellular life on Earth can be classified into one of the three domains: bacteria, archaea or eukaryotes. Whereas cells of bacteria and archaea are small and simple, those of eukaryotes are generally bigger and complex, containing a nucleus that encompasses DNA, and other subcellular compartments, referred to as organelles.</p

The α-proteobacteria: the Darwin finches of the bacterial world

The α-proteobacteria represent one of the most diverse bacterial subdivisions, displaying extreme variations in lifestyle, geographical distribution and genome size. Species for which genome data are available have been classified into a species tree based on a conserved set of vertically inherited core genes. By mapping the variation in gene content onto the species tree, genomic changes can be associated with adaptations to specific growth niches. Genes for adaptive traits are mostly located in ‘plasticity zones’ in the bacterial genome, which also contain mobile elements and are highly variable across strains. By physically separating genes for information processing from genes involved in interactions with the surrounding environment, the rate of evolutionary change can be substantially enhanced for genes underlying adaptation to new growth habitats, possibly explaining the ecological success of the α-proteo-bacterial subdivision

The Archaeal Roots of the Eukaryotic Dynamic Actin Cytoskeleton

It is generally well accepted that eukaryotes evolved from the symbiosis of an archaeal host cell and an alphaproteobacterium, a union that ultimately gave rise to the complex, eukaryotic cells we see today. However, the catalyst of this merger, the exact nature of the cellular biology of either partner, or how this event spawned the vast majority of complex life on Earth remains enigmatic. In recent years, the discovery of the Asgard archaea, the closest known prokaryotic relatives of eukaryotes, has been monumental for addressing these unanswered questions. These prokaryotes seem to encode an unprecedented number of genes related to features typically descriptive of eukaryotes, including intracellular trafficking, vesicular transport and a dynamic actin-based cytoskeleton. Collectively, these features imply that the Asgard archaea have the potential for cellular complexity previously thought to be unique to eukaryotes. Here, we review the most recent advances in our understanding of the archaeal cytoskeleton and its implications for determining the origin of eukaryotic cellular complexity. The transition from prokaryotic to eukaryotic cells represents a cornerstone event in the evolution of life on Earth. The actin cytoskeleton is one of many key features of eukaryotic cells. Here, Stairs and Ettema review the most recent advances in our understanding of the archaeal cytoskeleton and its implications for the origins of eukaryotes.</p