Plastid Genomes and Proteins Illuminate the Evolution of Eustigmatophyte Algae and Their Bacterial Endosymbionts

Abstract

Eustigmatophytes, a class of stramenopile algae (ochrophytes), include not only the extensively studied biotechnologically important genus Nannochloropsis but also a rapidly expanding diversity of lineages with much less well characterized biology. Recent discoveries have led to exciting additions to our knowledge about eustigmatophytes. Some proved to harbor bacterial endosymbionts representing a novel genus, Candidatus Phycorickettsia, and an operon of unclear function (ebo) obtained by horizontal gene transfer from the endosymbiont lineage was found in the plastid genomes of still other eustigmatophytes. To shed more light on the latter event, as well as to generally improve our understanding of the eustigmatophyte evolutionary history, we sequenced plastid genomes of seven phylogenetically diverse representatives (including new isolates representing undescribed taxa). A phylogenomic analysis of plastid genome-encoded proteins resolved the phylogenetic relationships among the main eustigmatophyte lineages and provided a framework for the interpretation of plastid gene gains and losses in the group. The ebo operon gain was inferred to have probably occurred within the order Eustigmatales, after the divergence of the two basalmost lineages (a newly discovered hitherto undescribed strain and the Pseudellipsoidion group). When looking for nuclear genes potentially compensating for plastid gene losses, we noticed a gene for a plastid-targeted acyl carrier protein that was apparently acquired by horizontal gene transfer from Phycorickettsia. The presence of this gene in all eustigmatophytes studied, including representatives of both principal clades (Eustigmatales and Goniochloridales), is a genetic footprint indicating that the eustigmatophyte–Phycorickettsia partnership started no later than in the last eustigmatophyte common ancestor.

Comparative Plastid Genomics of Non-Photosynthetic Chrysophytes: Genome Reduction and Compaction

“…Phylogenomic analysis using 40 plastid-encoded proteins showed a monophyletic assemblage of chrysophytes within stramenopiles with maximal support (posterior probability (PP)=1.00, maximum likelihood (ML)=100%, Supplementary Table S2). The chrysophyte assemblage formed a sister relationship with Eustigmatophyceae ( Figure 4A and Supplementary Figure S1), consistent with recently published studies suggesting that eustigmatophyte plastids are closely related to those of chrysophytes (Sěvcǐḱováet al, 2015;Han et al, 2019;Kim et al, 2019;Sěvcǐḱováet al, 2019). Our plastid phylogenomic investigations showed that the mixotrophic species Ochromonas sp.…”

Dictyochophyceae Plastid Genomes Reveal Unusual Variability in Their Organization

“…), but has also been lost repeatedly in other heterokont lineages (Ševčíková et al. ). This explanation, however, seems highly unlikely for dna B, which encodes DNA helicase involved in organelle division.…”

“…This gene is absent in almost all investigated ochrophyte plastid genomes (Ševčíková et al. ), and so far it has been found only in the plastid genome of the bolidophyte Triparma laevis (Tajima et al. ).…”

Toward Modern Classification of Eustigmatophytes, Including the Description of Neomonodaceae Fam. Nov. and Three New Genera1

“…The separate status of the Neomonodaceae is also supported by the recent phylogenomic analysis of multiple plastid genes including one representative of the group, Pseudellipsoidion edaphicum CAUP Q 404 (Ševčíková et al. ). The latter analysis placed P. edaphicum with maximal support as a sister lineage to the family Monodopsidaceae and the Eustigmataceae group combined, in agreement with our 18S rRNA gene phylogenies (Figs.…”

“…), which represents a novel separate lineage sister to all the previously known Eustigmatales including Neomonodaceae (see also the position of P. columelliferus , referred to as strain Mont 10/10‐1w, in the plastid phylogenomic analysis by Ševčíková et al. ). Thus, P. columelliferus may be the first encountered representative of a diverse eustigmatophyte clade for which a new formal taxon – perhaps a new family – may be established in the future.…”