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. 2021 Jan 25;21(1):11.
doi: 10.1186/s12862-020-01733-1.

The Rubisco small subunits in the green algal genus Chloromonas provide insights into evolutionary loss of the eukaryotic carbon-concentrating organelle, the pyrenoid

Affiliations

The Rubisco small subunits in the green algal genus Chloromonas provide insights into evolutionary loss of the eukaryotic carbon-concentrating organelle, the pyrenoid

Ryo Matsuzaki et al. BMC Ecol Evol. .

Abstract

Background: Pyrenoids are protein microcompartments composed mainly of Rubisco that are localized in the chloroplasts of many photosynthetic organisms. Pyrenoids contribute to the CO2-concentrating mechanism. This organelle has been lost many times during algal/plant evolution, including with the origin of land plants. The molecular basis of the evolutionary loss of pyrenoids is a major topic in evolutionary biology. Recently, it was hypothesized that pyrenoid formation is controlled by the hydrophobicity of the two helices on the surface of the Rubisco small subunit (RBCS), but the relationship between hydrophobicity and pyrenoid loss during the evolution of closely related algal/plant lineages has not been examined. Here, we focused on, the Reticulata group of the unicellular green algal genus Chloromonas, within which pyrenoids are present in some species, although they are absent in the closely related species.

Results: Based on de novo transcriptome analysis and Sanger sequencing of cloned reverse transcription-polymerase chain reaction products, rbcS sequences were determined from 11 strains of two pyrenoid-lacking and three pyrenoid-containing species of the Reticulata group. We found that the hydrophobicity of the RBCS helices was roughly correlated with the presence or absence of pyrenoids within the Reticulata group and that a decrease in the hydrophobicity of the RBCS helices may have primarily caused pyrenoid loss during the evolution of this group.

Conclusions: Although we suggest that the observed correlation may only exist for the Reticulata group, this is still an interesting study that provides novel insight into a potential mechanism determining initial evolutionary steps of gain and loss of the pyrenoid.

Keywords: Chloromonas; Evolution; Green algae; Hydrophobicity of RBCS helices; Pyrenoid; Pyrenoid loss; Rubisco small subunit (RBCS).

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Conflict of interest statement

The authors declare that they have no competing interests.

Figures

Fig. 1
Fig. 1
Bayesian phylogenetic tree of the Reticulata group of the genus Chloromonas based on the combined 7,109-bp data matrix for nuclear 18S and 28S ribosomal DNA, atpB, psaA, psaB, and ITS-2 sequences, showing evolution of pyrenoids. Numbers shown in top left, top right, bottom left, and bottom right exhibit posterior probabilities (0.95 or more) from Bayesian inference and bootstrap values (50% or more) from maximum likelihood, maximum parsimony, and neighbor-joining analyses, respectively. Presence (+) or absence (−) of pyrenoids in the Reticulata group is based on the previous light and electron microscopic studies [–18]. Pyrenoid loss was deduced by using Mesquite V3.6 [47]. In light microscopic photographs, vegetative cells of C. chlorococcoides strain SAG 15.82 and C. reticulata strain SAG 29.83 are shown, bars represent 5 μm and an arrow indicates a pyrenoid
Fig. 2
Fig. 2
Phylogenetic analysis of rbcS sequences from the Reticulata group. The tree was constructed based on maximum likelihood method using 307 base pairs of coding regions of rbcS (Table 1). Numbers at the branches indicate bootstrap values (50% or more). For details, see Methods of the main text
Fig. 3
Fig. 3
Box-whisker/bee swarm plots comparing the distribution of hydrophobicity of helices A and B from RBCS homologs of the Chlamydomonadales (Table 1). Significant difference (p < 0.001) is based on Brunner–Munzel test. a Comparison among five species of the Reticulata group of the genus Chloromonas. b Comparison among three groups of Chloromonadinia (the most left three), and 12 other lineages (11 strongly supported primary clades and Spermatozopsis [14]) within the Chlamydomonadales (Table 1), showing phylogeny based on Nakada et al. [14], Lemieux et al. [24] and Matsuzaki et al. [22, 27]
Fig. 4
Fig. 4
Amino acid alignment of helices A and B of RBCS homologs from the Reticulata group and Chlamydomonas reinhardtii (Table 1). Dot means that amino acid in the position is the same as that in the top sequence. Eliminated amino acids by less than 15% exposure ratio are grayed-out. The first position of helix B was alanine in all of the RBCS sequences from Chloromonas chlorococcoides, while proline in that from C. reticulata (surrounded by the red solid-line frames)

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