Dinoflagellate chloroplasts as a model for extreme genome reduction and fragmentation in organelles - The COCOA principle for gene retention.

The genomes of peridinin-containing dinoflagellate chloroplasts have a very unusual organisation. These genomes are highly fragmented and greatly reduced, with most of the usual complement of chloroplast genes relocated to the nucleus. Dinoflagellate chloroplasts highlight evolutionary changes that are found to varying extents in a number of other organelle genomes.

Publisher Correction: Genetic tool development in marine protists: emerging model organisms for experimental cell biology.

An amendment to this paper has been published and can be accessed via a link at the top of the paper.

Genetic tool development in marine protists: emerging model organisms for experimental cell biology.

Diverse microbial ecosystems underpin life in the sea. Among these microbes are many unicellular eukaryotes that span the diversity of the eukaryotic tree of life. However, genetic tractability has been limited to a few species, which do not represent eukaryotic diversity or environmentally relevant taxa.

Integrated Genomic and Transcriptomic Analysis of the Peridinin Dinoflagellate Amphidinium carterae Plastid.

The plastid genomes of peridinin-containing dinoflagellates are highly unusual, possessing very few genes, which are located on small chromosomal elements termed "minicircles". These minicircles may contain genes, or no recognisable coding information. Transcripts produced from minicircles may undergo unusual processing events, such as the addition of a 3' poly(U) tail.

The genetic intractability of Symbiodinium microadriaticum to standard algal transformation methods.

Modern transformation and genome editing techniques have shown great success across a broad variety of organisms. However, no study of successfully applied genome editing has been reported in a dinoflagellate despite the first genetic transformation of Symbiodinium being published about 20 years ago. Using an array of different available transformation techniques, we attempted to transform Symbiodinium microadriaticum (CCMP2467), a dinoflagellate symbiont of reef-building corals, with the view to performing subsequent CRISPR-Cas9 mediated genome editing.

Assessing Symbiodinium diversity in scleractinian corals via next-generation sequencing-based genotyping of the ITS2 rDNA region.

The persistence of coral reef ecosystems relies on the symbiotic relationship between scleractinian corals and intracellular, photosynthetic dinoflagellates in the genus Symbiodinium. Genetic evidence indicates that these symbionts are biologically diverse and exhibit discrete patterns of environmental and host distribution. This makes the assessment of Symbiodinium diversity critical to understanding the symbiosis ecology of corals.

The chloroplast genome of a Symbiodinium sp. clade C3 isolate.

Dinoflagellate algae of the genus Symbiodinium form important symbioses within corals and other benthic marine animals. Dinoflagellates possess an extremely reduced plastid genome relative to those examined in plants and other algae. In dinoflagellates the plastid genes are located on small plasmids, commonly referred to as 'minicircles'.

Polyuridylylation and processing of transcripts from multiple gene minicircles in chloroplasts of the dinoflagellate Amphidinium carterae.

Although transcription and transcript processing in the chloroplasts of plants have been extensively characterised, the RNA metabolism of other chloroplast lineages across the eukaryotes remains poorly understood. In this paper, we use RT-PCR to study transcription and transcript processing in the chloroplasts of Amphidinium carterae, a model peridinin-containing dinoflagellate. These organisms have a highly unusual chloroplast genome, with genes located on multiple small 'minicircle' elements, and a number of idiosyncratic features of RNA metabolism including transcription via a rolling circle mechanism, and 3' terminal polyuridylylation of transcripts.

Organization and expression of organellar genomes.

Protist mitochondrial genomes show a very wide range of gene content, ranging from three genes for respiratory chain components in Apicomplexa and dinoflagellates to nearly 100 genes in Reclinomonas americana. In many organisms the rRNA genes are fragmented, although still functional. Some protist mitochondria encode a full set of tRNAs, while others rely on imported molecules.

Dinoflagellates: a mitochondrial genome all at sea.

Dinoflagellate algae are notorious for their highly unusual organization of nuclear and chloroplast genomes. Early studies on the dinoflagellate mitochondrial genome indicated that it encodes the same three protein-coding genes found in Plasmodium spp., but with a complex organization and transcript editing.

A role for SENSITIVE TO FREEZING2 in protecting chloroplasts against freeze-induced damage in Arabidopsis.

The sensitive to freezing2 (SFR2) gene has an important role in freezing tolerance in Arabidopsis thaliana. We show that homologous genes are present, and expressed, in a wide range of terrestrial plants, including species not able to tolerate freezing. Expression constructs derived from the cDNAs of a number of different plant species, including examples not tolerant to freezing, are able to complement the freezing sensitivity of the Arabidopsis sfr2 mutant.

The remarkable chloroplast genome of dinoflagellates.

Dinoflagellates are an economically and ecologically important eukaryotic algal group. The organization of their chloroplast genome appears to be radically different from that in plants and other algae. The gene content has been dramatically reduced in dinoflagellates, with the large-scale transfer of genes to the nucleus.

Transcript analysis of dinoflagellate plastid gene minicircles.

The dinoflagellate chloroplast genome is fragmented into a number of plasmid-like minicircles, mostly containing one or more genes, and with a conserved core. We show here that, in addition to the transcripts of similar sizes to individual genes that have been reported previously, there are larger transcripts beginning and ending close to the core region. These may give rise to the smaller transcripts by processing.

Organization of the mitochondrial genome in the dinoflagellate Amphidinium carterae.

We have characterized the mitochondrial genome of the dinoflagellate Amphidinium carterae. It contains just 3 identifiable protein-coding genes: cox1, cox3, and cob. No evidence for rRNA or tRNA genes was found.

Comparative analysis of dinoflagellate chloroplast genomes reveals rRNA and tRNA genes.

Background: Peridinin-containing dinoflagellates have a highly reduced chloroplast genome, which is unlike that found in other chloroplast containing organisms. Genome reduction appears to be the result of extensive transfer of genes to the nuclear genome. Unusually the genes believed to be remaining in the chloroplast genome are found on small DNA 'minicircles'.

Molecular diversity of dinoflagellate symbionts of Cnidaria: the psbA minicircle of Symbiodinium.

Dinoflagellate algae of the genus Symbiodinium are important symbionts within corals and other benthic marine animals. The molecular diversity of Symbiodinium has been described mainly by use of ribosomal DNA sequence data. We tested whether minicircle sequences, which appear to form the chloroplast genome in many dinoflagellates, could be used as a marker for molecular diversity among symbionts found in corals and sea anemones.

Why are plastid genomes retained in non-photosynthetic organisms?

The evolution of the plastid from a photosynthetic bacterial endosymbiont involved a dramatic reduction in the complexity of the plastid genome, with many genes either discarded or transferred to the nucleus of the eukaryotic host. However, this evolutionary process has not gone to completion and a subset of genes remains in all plastids examined to date. The various hypotheses put forward to explain the retention of the plastid genome have tended to focus on the need for photosynthetic organisms to retain a genetic system in the chloroplast, and they fail to explain why heterotrophic plants and algae, and the apicomplexan parasites all retain a genome in their non-photosynthetic plastids.

Ammonia-oxidizing bacteria respond to multifactorial global change.

Recent studies have demonstrated that multiple co-occurring global changes can alter the abundance, diversity, and productivity of plant communities. Below ground processes, often mediated by soil microorganisms, are central to the response of these communities to global change. Very little is known, however, about the effects of multiple global changes on microbial communities.

Novel plastid gene minicircles in the dinoflagellate Amphidinium operculatum.

Seven new minicircles, forming part of the fragmented plastid genome of the dinoflagellate Amphidinium operculatum, have been identified by PCR. Three minicircles are full-length, one of 2.6 kb encoding the 23S rRNA gene, one of 2.

Phylogenetics of artificial manuscripts.

Biological evolution has parallels with the development of natural languages, man-made artifacts, and manuscript texts. As a result, phylogenetic methods developed for evolutionary biology are increasingly being used in linguistics, anthropology, archaeology, and textual criticism. Despite this popularity, there have been few critical tests of their suitability.

Evolution of the chloroplast genome.

We discuss the suggestion that differences in the nucleotide composition between plastid and nuclear genomes may provide a selective advantage in the transposition of genes from plastid to nucleus. We show that in the adenine, thymine (AT)-rich genome of Borrelia burgdorferi several genes have an AT-content lower than the average for the genome as a whole. However, genes whose plant homologues have moved from plastid to nucleus are no less AT-rich than genes whose plant homologues have remained in the plastid, indicating that both classes of gene are able to support a high AT-content.