The plastid genome of some eustigmatophyte algae harbours a bacteria-derived six-gene cluster for biosynthesis of a novel secondary metabolite

Abstract

Acquisition of genes by plastid genomes (plastomes) via horizontal gene transfer (HGT) seems to be a rare phenomenon. Here, we report an interesting case of HGT revealed by sequencing the plastomes of the eustigmatophyte algae Monodopsis sp. MarTras21 and Vischeria sp. CAUP Q 202. These plastomes proved to harbour a unique cluster of six genes, most probably acquired from a bacterium of the phylum Bacteroidetes, with homologues in various bacteria, typically organized in a conserved uncharacterized putative operon. Sequence analyses of the six proteins encoded by the operon yielded the following annotation for them: (i) a novel family without discernible homologues; (ii) a new family within the superfamily of metallo-dependent hydrolases; (iii) a novel subgroup of the UbiA superfamily of prenyl transferases; (iv) a new clade within the sugar phosphate cyclase superfamily; (v) a new family within the xylose isomerase-like superfamily; and (vi) a hydrolase for a phosphate moiety-containing substrate. We suggest that the operon encodes enzymes of a pathway synthesizing an isoprenoid–cyclitol-derived compound, possibly an antimicrobial or other protective substance. To the best of our knowledge, this is the first report of an expansion of the metabolic capacity of a plastid mediated by HGT into the plastid genome.

A gene transfer event suggests a long-term partnership between eustigmatophyte algae and a novel lineage of endosymbiotic bacteria

“…CAUP Q 202 and Monodopsis sp. MarTras21 [ 29 ]. The ebo operon in Phycorickettsia has the same architecture as the one in the two plastid genomes and in some bacterial groups, particularly Bacteroidetes and Cyanobacteria (Supplementary Figure 4 ), that is, is of the “ABCDEF type” (the letters reflect the order of the six ebo genes; see [ 29 ]).…”

“…MarTras21 [ 29 ]. The ebo operon in Phycorickettsia has the same architecture as the one in the two plastid genomes and in some bacterial groups, particularly Bacteroidetes and Cyanobacteria (Supplementary Figure 4 ), that is, is of the “ABCDEF type” (the letters reflect the order of the six ebo genes; see [ 29 ]). The identification of the ebo operon in Phycorickettsia is indeed noteworthy, as we detected neither the operon as a whole nor homologues of individual ebo genes in any other member of Rickettsiales with the genome sequence available.…”

“…MarTras21 belonging to the second main eustigmatophyte clade, Eustigmatales [ 27 ]. We have previously reported sequences of organellar genomes of all three algae [ 27 – 29 ]. The most striking finding, directly relevant to the present study, was the identification of a novel six-gene operon in the plastid genomes of Vischeria and Monodopsis [ 29 ].…”

“…We have previously reported sequences of organellar genomes of all three algae [ 27 – 29 ]. The most striking finding, directly relevant to the present study, was the identification of a novel six-gene operon in the plastid genomes of Vischeria and Monodopsis [ 29 ]. Comparative genomic and phylogenetic analyses revealed that this operon, denoted ebo (eustigmatophyte-bacterial operon), is widespread in different groups of bacteria and was horizontally transferred into an ancestor of Vischeria and Monodopsis .…”

“…Comparative genomic and phylogenetic analyses revealed that this operon, denoted ebo (eustigmatophyte-bacterial operon), is widespread in different groups of bacteria and was horizontally transferred into an ancestor of Vischeria and Monodopsis . The function of this operon remains unknown, but bioinformatic analyses of the six encoded proteins revealed most of them as putative enzymes underpinning the synthesis of an unknown prenylated cyclitol or its derivative [ 29 ].…”