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Functional type 2 photosynthetic reaction centers found in the rare bacterial phylum Gemmatimonadetes - PubMed

Yonghui Zeng  1 ,

Functional type 2 photosynthetic reaction centers found in the rare bacterial phylum Gemmatimonadetes

Yonghui Zeng et al. Proc Natl Acad Sci U S A. .

Abstract

Photosynthetic bacteria emerged on Earth more than 3 Gyr ago. To date, despite a long evolutionary history, species containing (bacterio)chlorophyll-based reaction centers have been reported in only 6 out of more than 30 formally described bacterial phyla: Cyanobacteria, Proteobacteria, Chlorobi, Chloroflexi, Firmicutes, and Acidobacteria. Here we describe a bacteriochlorophyll a-producing isolate AP64 that belongs to the poorly characterized phylum Gemmatimonadetes. This red-pigmented semiaerobic strain was isolated from a freshwater lake in the western Gobi Desert. It contains fully functional type 2 (pheophytin-quinone) photosynthetic reaction centers but does not assimilate inorganic carbon, suggesting that it performs a photoheterotrophic lifestyle. Full genome sequencing revealed the presence of a 42.3-kb-long photosynthesis gene cluster (PGC) in its genome. The organization and phylogeny of its photosynthesis genes suggests an ancient acquisition of PGC via horizontal transfer from purple phototrophic bacteria. The data presented here document that Gemmatimonadetes is the seventh bacterial phylum containing (bacterio)chlorophyll-based phototrophic species. To our knowledge, these data provide the first evidence that (bacterio)chlorophyll-based phototrophy can be transferred between distant bacterial phyla, providing new insights into the evolution of bacterial photosynthesis.

Keywords: aerobic photoheterotroph; anoxygenic photosynthesis; bacterial pigments; fluorescence imaging system; horizontal gene transfer.

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Conflict of interest statement

The authors declare no conflict of interest.

Figures

Fig. 1.

Microscopy images of the phototrophic Gemmatimonadetes strain AP64 and 16S rRNA gene phylogeny showing the position of the Gemmatimonadetes phylum among the Bacteria domain. (A, Left) Infrared epifluorescence microscopy image (false colors). (Center) Scanning electron microscopy image. (Right) Transmission electron microscopy image of an AP64 cell. (B) phylogenetic tree of 16S rRNA genes based on the data from the All Species Living Tree project (

www.arb-silva.de/

). Orange wedges indicate the bacterial phyla that contain chlorophototrophic species. Scale bar represents changes per position.

Fig. 2.

Gene organization of the PGC of AP64 in comparison with Proteobacteria and Firmicutes. Genome data were referenced for the PGC composition: R. capsulatus SB1003 (GenBank accession no. CP001312), R. gelatinosus IL144 (GenBank accession no. AP012320), and H. modesticaldum Ice1 (GenBank accession no. CP000930). bch (green), bacteriochlorophyll biosynthesis genes; puh (pink), genes encoding reaction center assembly proteins; puf (red), genes encoding reaction center proteins; crt (brownish yellow), carotenoid biosynthesis genes; gray, photosynthesis nonrelated genes or hypothetical ORFs.

Fig. 3.

Photosystem functionality and pigment characterization of strain AP64. (A) In vivo absorption spectrum. (Inset) The 77K fluorescence emission spectrum. (B) Fluorescence induction and relaxation kinetics recorded by infrared fluorometry. (C) HPLC elution profile of pigment extracts from strains Gemmatimonas sp. AP64 and G. aurantiaca T-27 at 480 nm for carotenoids and 770 nm for BChl a. Note that traces are shifted vertically. Numbers above peaks indicate main pigments: 1 and 2, putative (2S,2’S)-oscillol 2,2’-di-(α-

l

-rhamnoside) (29); 3–6, unknown carotenoids; 7, BChl aGG (geranlylgeranyl); 8, spirilloxanthin; 9, BChl aP (phytol); 10, bacteriophaeophytin aP.

Fig. 4.

Phylogenetic analysis of Gemmatimonadetes AcsF-like protein sequences predicted from environmental metagenomes in relation to other phototrophic bacterial phyla. Environmental Gemmatimonadetes AcsF-like sequences were retrieved from the CAMERA or NCBI WGS databases using tblastn searching (

SI Appendix, Table S8

). Pairwise deletion was performed at the sites containing missing data or alignment gaps. The unrooted tree was inferred using a neighbor-joining algorithm with 1,000 resamplings. Bootstrap values >50% are shown. Ylake, Yellowstone Lake. The total number of amino acids of the partial Gemmatimonadetes AcsF-like ORFs are shown next to the names. CAMERA/GenBank accession numbers are in parentheses.

Fig. 5.

Phylogenetic analyses of AP64 photosynthesis genes. (Left ) Analysis based on concatenated alignments of amino acid sequences of magnesium chelatase (BchIDH/ChlIDH; 1,810 common amino acid positions). (Center) Analysis based on concatenated alignments of amino acid sequences of light independent protochlorophyllide reductase (BchLNB/ChlLNB; 921 common amino acid positions). (Right) Analysis based on concatenated alignments of amino acid sequences of the photosynthetic reaction center subunits (PufLM; 507 common amino acid positions). Maximum likelihood (ML) and neighbor-joining (NJ) trees were inferred for strain AP64 and representative species from other six phototrophic phyla. The PufLM tree was rooted by Chroococcidiopsis thermalis (Cyanobacteria) D1/D2 sequences. ML/NJ bootstrap values >50% are shown on the trees. Scale bars represent changes per position.

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