The case of horizontal gene transfer from bacteria to the peculiar dinoflagellate plastid genome

Abstract

Organelle genomes lose their genes by transfer to host nuclear genomes, but only occasionally are enriched by foreign genes from other sources. In contrast to mitochondria, plastid genomes are especially resistant to such horizontal gene transfer (HGT), and thus every gene acquired in this way is notable. An exceptional case of HGT was recently recognized in the peculiar peridinin plastid genome of dinoflagellates, which is organized in plasmid-like minicircles. Genomic and phylogenetic analyses of Ceratium horridum and Pyrocystis lunula minicircles revealed four genes and one unannotated open reading frame that probably were gained from bacteria belonging to the Bacteroidetes. Such bacteria seem to be a good source of genes because close endosymbiotic associations between them and dinoflagellates have been observed. The HGT-acquired genes are involved in plastid functions characteristic of other photosynthetic eukaryotes, and their arrangement resembles bacterial operons. These studies indicate that the peridinin plastid genome, usually regarded as having resulted from reduction and fragmentation of a typical plastid genome derived from red algae, may have a chimeric origin that includes bacterial contributions. Potential contamination of the Ceratium and Pyrocystis plastid genomes by bacterial sequences and the controversial localization of their minicircles in the nucleus are also discussed.

The chloroplast genomes of Bryopsis plumosa and Tydemania expeditiones (Bryopsidales, Chlorophyta): compact genomes and genes of bacterial origin

“…The presence of bacterial genes (including genes involved in mobile functions) in both the Bryopsis and Tydemania cpDNAs, and absent in other green algae, suggest that these genes have been acquired through horizontal gene transfer. Transfer of genes to plastid genomes is only rarely observed but some clear instances are known [ 36 , 37 ]. In the Oedogonium chloroplast genome, the unprecedented finding of int (a gene belonging to the family of tyrosine recombinases) and dpoB (a member of the B family of DNA-directed DNA polymerases) was seen as evidence of horizontal transfer, possibly from a mitochondrial genome donor [ 99 ].…”

“…In the cpDNA of Nephroselmis olivacea , two large regions (27 kb in total) are believed to have been acquired by lateral transfer from a bacterial donor based on a deviant base composition, the lack of genes typically found in cpDNAs, and the presence of an ORF showing similarity to phage associated DNA primases [ 9 , 38 ]. Horizontal gene transfer from bacteria to plastids has also been demonstrated in other groups of algae, including red algae [ 39 ], dinoflagellates [ 37 , 40 ], haptophytes and cryptophytes [ 41 , 42 ]. It is relevant to note that siphonous green algae (Bryopsidales) are known to harbor intracellular bacterial communities, with some bacteria showing close associations with the host (e.g., [ 43 - 45 ]).…”

Monophyly of Archaeplastida supergroup and relationships among its lineages in the light of phylogenetic and phylogenomic studies. Are we close to a consensus?

“…The best known is the ribosomal protein rpl36 gene, which was transferred from a proteobacterium or a planctomycete bacterium to plastid genomes of cryptophytes and haptophytes [180]. The other examples are genes encoding the large and small subunits of RuBisCO form I, acquired by the primary plastid genome of the common ancestor of red algae from a proteobacterium [152] (for additional cases, see [181,182] and references therein).…”

Transcription factors in microalgae: genome-wide prediction and comparative analysis

“…Multiple endosymbiosis resulting in the algal diversity [ 18 ] is punctuated by numerous gene transfer events. These gene transfer events comprise both EGT [ 115 , 116 ], as the original case of HGT from bacteria to the plastid genome [ 117 ], or from bacteria or archaebacteria to the nuclear genome [ 40 , 105 , 118 , 119 ]. In these HGT, the donor organism is prokaryotic, but interesting cases of HGT from a fungus to an alga were recently shown [ 120 ].…”