Abstract
AbstractThe theory envisaging the origin of plastids from endosymbiotic cyanobacteria is well-established but it is difficult to explain the evolution (spread) of plastids in phylogenetically diverse plant groups. It is widely believed that primordial endosymbiosis occurred in the last common ancestor of all algae^1^, which then diverged into the three primary photosynthetic eukaryotic lineages, viz. the Rhodophyta (red algae), Glaucocystophyta (cyanelle-containing algae) and Viridiplantae (green algae plus all land plants)^2^. Members of these three groups invariably have double membrane-bound plastids^3^, a property that endorses the primary endosymbiotic origin of the organelles. On the other hand, the three or four membrane-bound plastids of the evolutionary complicated Chromalveolates [chromista (cryptophytes, haptophytes, and stramenopiles) and alveolata (dinoflagellates, apicomplexans, and ciliates)] are inexplicable in the light of a single endosymbiosis event, thereby necessitating the postulation of the secondary^4,5^ and tertiary^6^ endosymbiosis theories where a nonphotosynthetic protist supposedly engulfed a red or a green alga^7^ and an alga containing a secondary plastid itself was engulfed^8^ respectively. In the current state of understanding, however, there is no clue about the taxonomic identity of the cyanobacterial ancestor of chloroplasts, even though there is a wide consensus on a single primordial endosymbiosis event. During our metagenomic investigation of a photosynthetic geothermal microbial mat community we discovered a novel order-level lineage of Cyanobacteria that - in 16S rRNA gene sequence-based phylogeny - forms a robust monophyletic clade with chloroplast-derived sequences from diverse divisions of Viridiplantae. This cluster diverged deeply from the other major clade encompassing all hitherto known groups of Cyanobacteria plus the chloroplasts of Rhodophyta, Glaucocystophyceae and Chromalveolates. Since this fundamental dichotomy preceded the origin of all chloroplasts, it appears that two early-diverging cyanobacterial lineages had possibly given rise to two discrete chloroplast descents via two separate engulfment events.
Highlights
The theory envisaging the origin of plastids from endosymbiotic cyanobacteria is well-established but it is difficult to explain the evolution of plastids in phylogenetically diverse plant groups
In the current state of understanding, there is no clue about the taxonomic identity of the cyanobacterial ancestor of chloroplasts, even though there is a wide consensus on a single primordial endosymbiosis event
Among the hitherto known groups of Cyanobacteria (HKGC), members of Oscillatoriales, Nostocales and Pleurocapsales had maximum (87-89%, or even lower) 16S rDNA sequence similarities with the new phylotype, whereas other groups like Gloeobacterales, Chroococcales, Stigonematales and Prochlorophytes had 85-87%, or lower, similarity levels. 16S rDNA from chloroplasts of Glaucocystophyceaea, Rhodophyta and Chromalveolates respectively had ≤89%, ≤87% and ≤88 % sequence similarities with the homologs from the new phylotype (Fig. 2)
Summary
The theory envisaging the origin of plastids from endosymbiotic cyanobacteria is well-established but it is difficult to explain the evolution (spread) of plastids in phylogenetically diverse plant groups. During our metagenomic investigation of a photosynthetic geothermal microbial mat community we discovered a novel order-level lineage of Cyanobacteria that - in 16S rRNA gene sequence-based phylogeny - forms a robust monophyletic clade with chloroplastderived sequences from diverse divisions of Viridiplantae This cluster diverged deeply from the other major clade encompassing all hitherto known groups of Cyanobacteria plus the chloroplasts of Rhodophyta, Glaucocystophyceae and Chromalveolates. While the CT-specific 35-mer oligonucleotide primer did not hybridize with standard bacterial cultures (data not shown), a blank having the CT-specific probe but notyramide signal amplification reagent resulted in fluorescence of the filamentous cells with intensities equivalent to their autofluorescence observed in LSCM with 488 nm excitation and emission detection at long pass (LP) 560 nm or LP 615 nm (Fig. 1H & I) In this set, no image was obtained below 545 nm emission detection. Our observations offered no reason to believe that the remote ancestor of Candidatus Thermofiliformales, though closely related to the progenitor of green plant chloroplasts, was the source of Chlb in evolution
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