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, 8 (1), 9142

A Novel Species of the Marine Cyanobacterium Acaryochloris With a Unique Pigment Content and Lifestyle

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A Novel Species of the Marine Cyanobacterium Acaryochloris With a Unique Pigment Content and Lifestyle

Frédéric Partensky et al. Sci Rep.

Abstract

All characterized members of the ubiquitous genus Acaryochloris share the unique property of containing large amounts of chlorophyll (Chl) d, a pigment exhibiting a red absorption maximum strongly shifted towards infrared compared to Chl a. Chl d is the major pigment in these organisms and is notably bound to antenna proteins structurally similar to those of Prochloron, Prochlorothrix and Prochlorococcus, the only three cyanobacteria known so far to contain mono- or divinyl-Chl a and b as major pigments and to lack phycobilisomes. Here, we describe RCC1774, a strain isolated from the foreshore near Roscoff (France). It is phylogenetically related to members of the Acaryochloris genus but completely lacks Chl d. Instead, it possesses monovinyl-Chl a and b at a b/a molar ratio of 0.16, similar to that in Prochloron and Prochlorothrix. It differs from the latter by the presence of phycocyanin and a vestigial allophycocyanin energetically coupled to photosystems. Genome sequencing confirmed the presence of phycobiliprotein and Chl b synthesis genes. Based on its phylogeny, ultrastructural characteristics and unique pigment suite, we describe RCC1774 as a novel species that we name Acaryochloris thomasi. Its very unusual pigment content compared to other Acaryochloris spp. is likely related to its specific lifestyle.

Conflict of interest statement

The authors declare no competing interests.

Figures

Figure 1
Figure 1
Maximum likelihood phylogenetic tree based on the 16S rRNA gene showing the position of the new RCC1774 strain compared to a diverse selection of freshwater and marine cyanobacteria. Green oxyphotobacteria are highlighted in green, while Acaryochloris spp. are shown in orange and the new strain in red. Numbers shown at nodes correspond to bootstrap values for ML, NJ analyses and Bayesian posterior probabilities (PP; ranging between 0 and 1), respectively. Only values higher than 60% for bootstrap analyses and 0.60 for PP are shown on the phylogenetic tree. For each strain, the sequence accession number of the 16S rRNA gene (or genome, if not available) is indicated between brackets. The scale bar represents 0.025 substitution per nucleotide.
Figure 2
Figure 2
Comparative HPLC analysis of the pigment content of RCC1774 and the control Chl d-containing strain Acaryochloris sp. HCIR111A. (a,b) Chromatograms using the method described by Zapata and co-workers. Pigments shared by the two strains (i.e. same retention time and absorption spectrum) are indicated by numbers: 1, Mg-2,4-divinyl pheoporphyrin a5; 2, possible caloxanthin (monohydroxy-zeaxanthin); 3, zeaxanthin; 4, 5 & 7, unidentified carotenoids; 6, Chl a; 8 β,ε-carotene (a.k.a. α-carotene). RCC1774-specific pigments: a, Chlide a; b, possible nostoxanthin; c & d, unidentified carotenoids; e, Chl b. HCIR111A-specific pigments: a′ & b′, Chlide d-like pigments; c′ & d′, unidentified carotenoids; e′, Chl d. (c,d) On-line absorption spectra of Chl b (RCC1774) and Chl d (HCIR111A); for other peaks, see Supplementary Fig. S2.
Figure 3
Figure 3
Whole cell absorption spectra of RCC1774 and the control strains Acaryochloris sp. HCIR111A and Synechococcus sp. RS9917. Prior to measurement, cells were disrupted using a French press to reduce light scattering.
Figure 4
Figure 4
Characterization of water soluble extracts from cells of RCC1774 and the control strain Synechococcus sp. RS9917 separated by ultracentrifugation on a sucrose gradient. (a) Photograph of the blue-colored fractions obtained for RS9917 (left) and RCC1774 (right). (b) Absorption spectrum of the different fractions. (c,d) Excitation (plain lines) and emission spectra (dashed lines) of the different fractions obtained for RS9917 (c) and RCC1774 (d).
Figure 5
Figure 5
(a) Culture flasks of RCC1774 (left) and HCIR111A (right) showing their distinct colour. (b,c) Colour light micrographs of RCC1774 (a) and HCIR111A (b) using differential interference contrast (DIC). (d,g) Black and white light micrographs of RCC1774 (d) and HCIR111A (g) under DIC. (e,f) The same cells of RCC1774 (e,f) and HCIR111A (h,i) seen under epifluorescence using blue (e,h) and green (f,i) excitation. Arrows indicate three large or dividing cells that brightly fluoresce under blue (note the curtain-like organization of thylakoids) but comparatively less under green excitation. (j) Box plot chart showing the cell size distribution (n = 100) for each strain. The bold line indicates the median.
Figure 6
Figure 6
Flow cytograms of a mixture of RCC1774 and the control Acaryochloris sp. HCIR111A cultures. (a) Forward scatter vs. Side scatter cytogram. (b) Red fluorescence from the red laser (633 nm, exciting C-PC) vs. red fluorescence from the blue laser (488 nm, exciting Chls).
Figure 7
Figure 7
TEM images of RCC1774 (ac) and the control Acaryochloris sp. strain HCIR111A (d,e). (a,d) Groups of cells; (c,e) Individual cells; (b) Detail of a RCC1774 cell. Abbreviations: Ca, carboxysomes, Nu, nucleoid; LG, lipid granules; Th, thylakoids.

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