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

Zeng, Yonghui; Feng, Fan; Medová, Hana; Dean, Jason; Koblížek, Michal

doi:10.1073/pnas.1400295111

Cited by 219 publications

(275 citation statements)

References 58 publications

(51 reference statements)

Supporting

Mentioning

262

Contrasting

Order By: Relevance

“…At the same time, the nearness of the Chlorobi to Acidobacteria and Proteobacteira is also consistent with the ChlorobiBacteroidetes-Fibrobacterere supergroup bifurcating prior to the radiation of the Proteobacteria (Wu and Eisen 2008, Jun et al 2010, David and Alm 2011, Segata et al 2013, Marin et al 2017. Similarly, the phylogenetic proximity of the Gemmatimonadetes to the Chlorobi has also been demonstrated (Segata et al 2013, Zeng et al 2014, which is consistent with this group obtaining Type II reaction centres via horizontal gene transfer from the Proteobacteria (Zeng et al 2014).…”

Section: Resultssupporting

confidence: 71%

Early emergence of the FtsH proteases involved in photosystem II repair

Shao¹,

Cardona²,

Nixon³

2018

Photosynt.

View full text Add to dashboard Cite

Efficient degradation of damaged D1 during the repair of PSII is carried out by a set of dedicated FtsH proteases in the thylakoid membrane. Here we investigated whether the evolution of FtsH could hold clues to the origin of oxygenic photosynthesis. A phylogenetic analysis of over 6000 FtsH protease sequences revealed that there are three major groups of FtsH proteases originating from gene duplication events in the last common ancestor of bacteria, and that the FtsH proteases involved in PSII repair form a distinct clade branching out before the divergence of FtsH proteases found in all groups of anoxygenic phototrophic bacteria. Furthermore, we showed that the phylogenetic tree of FtsH proteases in phototrophic bacteria is similar to that for Type I and Type II reaction centre proteins. We conclude that the phylogeny of FtsH proteases is consistent with an early origin of photosynthetic water oxidation chemistry.

show abstract

Section: Resultssupporting

confidence: 71%

Early emergence of the FtsH proteases involved in photosystem II repair

Shao¹,

Cardona²,

Nixon³

2018

Photosynt.

View full text Add to dashboard Cite

show abstract

“…This inference can only be placed in relative time, but it is among the strongest pieces of evidence that illustrates that anoxygenic photosynthesis must be a very ancient metabolism (3). This does not indicate, however, that the taxa that do anoxygenic phototrophy today must be similarly ancient, due to the impact of HGT (8)(9)(10). It is also possible that anoxygenic photosynthesis evolved in stem group lineages that have gone extinct (3).…”

Section: Resultsmentioning

confidence: 99%

“…This possibility is supported by the observation that anoxygenic photosynthesis often sits within a derived position in the phyla in which it is found (3). Moreover, it is increasingly being recognized that horizontal gene transfer (HGT) has likely played a major role in the distribution of phototrophy (8)(9)(10). Together, these lines of evidence suggest that phototrophy may have first evolved in lineages that are either yet to be discovered or have gone extinct.…”

mentioning

confidence: 99%

Evolution of the 3-hydroxypropionate bicycle and recent transfer of anoxygenic photosynthesis into the Chloroflexi

Shih

Ward

Fischer

2017

Proc. Natl. Acad. Sci. U.S.A.

100

View full text Add to dashboard Cite

Various lines of evidence from both comparative biology and the geologic record make it clear that the biochemical machinery for anoxygenic photosynthesis was present on early Earth and provided the evolutionary stock from which oxygenic photosynthesis evolved ca. 2.3 billion years ago. However, the taxonomic identity of these early anoxygenic phototrophs is uncertain, including whether or not they remain extant. Several phototrophic bacterial clades are thought to have evolved before oxygenic photosynthesis emerged, including the Chloroflexi, a phylum common across a wide range of modern environments. Although Chloroflexi have traditionally been thought to be an ancient phototrophic lineage, genomics has revealed a much greater metabolic diversity than previously appreciated. Here, using a combination of comparative genomics and molecular clock analyses, we show that phototrophic members of the Chloroflexi phylum are not particularly ancient, having evolved well after the rise of oxygen (ca. 867 million years ago), and thus cannot be progenitors of oxygenic photosynthesis. Similarly, results show that the carbon fixation pathway that defines this clade-the 3-hydroxypropionate bicycleevolved late in Earth history as a result of a series of horizontal gene transfer events, explaining the lack of geological evidence for this pathway based on the carbon isotope record. These results demonstrate the role of horizontal gene transfer in the recent metabolic innovations expressed within this phylum, including its importance in the development of a novel carbon fixation pathway.carbon fixation | phototrophy | molecular clock | comparative genomics F rom both biological and geological data, it is widely thought that anoxygenic photosynthesis preceded the development of oxygenic photosynthesis and the rise of atmospheric oxygen (1). Although it has been largely accepted that oxygenic photosynthesis evolved in ancient Cyanobacterial lineages (2), very little is known about the nature and evolutionary history of anoxygenic phototrophy, with most of our understanding stemming from assumptions and hypotheses based on the few extant bacterial taxa that host this metabolism. Given the significance of the accumulation of oxygen ca. ∼2.3 billion years ago, it is of no surprise that the majority of efforts have focused on studying oxygenic photosynthesis. However, this has resulted in a paucity of studies critically examining basic and core questions on the origins of anoxygenic photosynthesis, such as what bacterial lineage developed this metabolism and when did it evolve? These questions are essential to our first-order knowledge of how early microbial metabolisms may have shaped the geochemical cycles of our planet.Although chlorophyll-based photosynthesis can be found in seven known bacterial phyla (i.e

show abstract

“…In addition, it is believed that acsF was horizontally transferred from cyanobacteria to Proteobacteria before the divergence of Alphaproteobacterial, Betaproteobacterial, and Gammaproteobacterial lineages, because cyanobacteria were initially oxygenating the atmosphere, conferring an advantage to anoxygenic phototrophs previously reliant solely on O 2 -sensitive BchE (26). A newly discovered bacterial phototroph belonging to the phylum Gemmatimonadetes is believed to have acquired an acsF-containing purple bacterial PGC via horizontal gene transfer (39), and thus is more recent than the acquisition of acsF by the Proteobacteria. The acsF gene is also found in Chloroflexi and the single phototrophic member of the phylum Acidobacteria discovered to date (28).…”

Section: Discussionmentioning

confidence: 99%

Three classes of oxygen-dependent cyclase involved in chlorophyll and bacteriochlorophyll biosynthesis

Chen

Canniffe

Hunter

2017

Proc. Natl. Acad. Sci. U.S.A.

View full text Add to dashboard Cite

The biosynthesis of (bacterio)chlorophyll pigments is among the most productive biological pathways on Earth. Photosynthesis relies on these modified tetrapyrroles for the capture of solar radiation and its conversion to chemical energy. (Bacterio)chlorophylls have an isocyclic fifth ring, the formation of which has remained enigmatic for more than 60 y. This reaction is catalyzed by two unrelated cyclase enzymes using different chemistries. The majority of anoxygenic phototrophic bacteria use BchE, an O 2 -sensitive [4Fe-4S] cluster protein, whereas plants, cyanobacteria, and some phototrophic bacteria possess an O 2 -dependent enzyme, the major catalytic component of which is a diiron protein, AcsF. Plant and cyanobacterial mutants in ycf54 display impaired function of the O 2 -dependent enzyme, accumulating the reaction substrate. Swapping cyclases between cyanobacteria and purple phototrophic bacteria reveals three classes of the O 2 -dependent enzyme. AcsF from the purple betaproteobacterium Rubrivivax (Rvi.) gelatinosus rescues the loss not only of its cyanobacterial ortholog, cycI, in Synechocystis sp. PCC 6803, but also of ycf54; conversely, coexpression of cyanobacterial cycI and ycf54 is required to complement the loss of acsF in Rvi. gelatinosus. These results indicate that Ycf54 is a cyclase subunit in oxygenic phototrophs, and that different classes of the enzyme exist based on their requirement for an additional subunit. AcsF is the cyclase in Rvi. gelatinosus, whereas alphaproteobacterial cyclases require a newly discovered protein that we term BciE, encoded by a gene conserved in these organisms. These data delineate three classes of O 2 -dependent cyclase in chlorophototrophic organisms from higher plants to bacteria, and their evolution is discussed herein.

show abstract

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

Cited by 219 publications

References 58 publications

Early emergence of the FtsH proteases involved in photosystem II repair

Early emergence of the FtsH proteases involved in photosystem II repair

Evolution of the 3-hydroxypropionate bicycle and recent transfer of anoxygenic photosynthesis into the Chloroflexi

Three classes of oxygen-dependent cyclase involved in chlorophyll and bacteriochlorophyll biosynthesis

Contact Info

Product

Resources

About