Plastid DNA from Pyrenomonas salina (Cryptophyceae): physical map, genes, and evolutionary implications

Abstract

Cryptomonads are thought to have arisen from a symbiotic association between a eukaryotic flagellated host and a eukaryotic algal symbiont, presumably related to red algae. As organellar DNAs have proven to be useful tools in elucidating phylogenetic relationships, the plastid (pt) DNA of the cryptomonad alga Pyrenomonas salina has been characterized in some detail. A restriction map of the circular 127 kb ptDNA from Pyrenomonas salina was established. An inverted repeat (IR) region of about 5 kb separates two single-copy regions of 15 and 102 kb, respectively. It contains the genes for the small and large subunit of rRNA. Ten protein genes, coding for the large subunit of ribulose-1,5-bisphosphate carboxylase, the 47 kDa, 43 kDa and 32 kDa proteins of photosystem II, the ribosomal proteins L2, S7 and S11, the elongation factor Tu, as well as the alpha- and beta-subunits of ATP synthase, have been localized on the restriction map either by hybridization of heterologous gene probes or by sequence homologies. The gene for the plastidal small subunit (SSUr) RNA has been sequenced and compared to homologous SSU regions from the cyanobacterium Anacystis nidulans and plastids from rhodophytes, chromophytes, euglenoids, chlorophytes, and land plants. A phylogenetic tree constructed with the neighborliness method and indicating a relationship of cryptomonad plastids with those of red algae is presented.

Substitution rate calibration of small subunit ribosomal RNA identifies chlorarachniophyte endosymbionts as remnants of green algae.

“…The cpDNA-encoded SSU rRNAs of the cryptomonads are grouped with those of algae containing chlorophyll c or phycobiliproteins, which is also in agreement with previous trees based on SSU rRNA (29,35,37). Since the cpDNAencoded SSU rRNA of Chlorarachnion does not cluster with the cpDNA-encoded SSU rRNA of cryptomonads, the hypothesis that the two groups of algae obtained their endosymbionts independently, is further supported.…”

“…Although not supported by bootstrap analysis in the tree of Fig. 1, this relationship has been suggested previously on the basis of SSU rRNA trees (1,27,29,30). Furthermore, like the red algae, cryptomonads contain phycobilins as accessory pigments.…”

Phylogenetic relationships among algae based on complete large-subunit rRNA sequences.

“…When the chlorarachniophyte NM is omitted from the analysis and only the cryptomonad NM is included (not shown), it forms an independent lineage, clearly separated from the green algae and land plants, which still form a very well-supported clade. However, on the basis of LSU rRNA, the red algal ancestry of the cryptomonad endosymbiont, as suggested previously (Douglas et al, 1991 ;Maier et al, 1991 ;Maerz et al, 1992 ;Van de Peer et al, 1996a) cannot be demonstrated. When only the chlorarachniophyte NM sequence is included, its phylogenetic position remains basically unchanged, but the bootstrap support for the clade formed by green algae plus land plants increases spectacularly (Fig.…”

“…Since the NM of cryptomonads and chlorarachniophytes still encode 18S rRNA, it could be demonstrated that the endosymbionts of chlorarachniophytes are probably related to green algae, while those of cryptomonads are most probably related to red algae ( Van de Peer et al, 1996a). Although the latter relationship is usually not supported by bootstrap analysis, it has been suggested previously on the basis of SSU rRNA (Douglas et al, 1991 ;Maier et al, 1991 ;Maerz et al, 1992). In haptophytes and heterokont algae, a remnant of the endosymbionts nucleus does not exist anymore and therefore the true nature of the endosymbiont that gave rise to their plastids can only be inferred through sequence analysis of plastid genes.…”

Goniomonas: rRNA sequences indicate that this phagotrophic flagellate is a close relative of the host component of cryptomonads

“…These trees suggest that the endosymbiont is most closely related to extant red algae, which is also consistent with the presence of phycobilin pigments and the site of starch storage in the endosymbionts and red algae (see McFadden, 1993, for review). In addition, phylogenetic trees inferred from sequences of plastid genes such as rbcL and 16S rRNA also suggest that the endosymbiont could share a common ancestry with red algae (Douglas et al, 1991a, Douglas & Turner 1991Maerz et al, 1992).…”