Whole-Genome Analysis of Photosynthetic Prokaryotes

Raymond, Jason; Zhaxybayeva, Olga; Gogarten, J. Peter; Gerdes, Sveta Y.; Blankenship, Robert E.

doi:10.1126/science.1075558

Cited by 247 publications

(173 citation statements)

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“…It is generally believed that the evolution of photosynthetic genes was accompanied by their dissemination by way of LGT between different groups of bacteria (12,26,30,31,56). This idea is supported by the apparent presence of nonphotosynthetic representatives in all of these phyla, except for Cyanobacteria; by the fact that the photosynthesis-related proteins are often encoded on a single contiguous chromosomal region (superoperon) (20,57); by several phylogenetic analyses (8,11,58); and by the observation that photosynthetic genes can be transduced by cyanophages (59).…”

Section: Evolution Of Photosynthesis and Lateral Gene Transfermentioning

confidence: 69%

“…We analyzed the phylogenetic affinities of genes in this set and identified previously unrecognized candidate photosynthetic genes. We further used this gene set to address the identity of the first phototrophs, a subject of intense discussion in recent years (8,9,. We show that cyanobacteria and plants share numerous photosynthesis-related genes that are missing in genomes of other phototrophs.…”

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confidence: 99%

“…demonstrated a wide variety of gene complements within this genus due to massive genome reduction in some lineages (6,7). Studies of the genes shared by cyanobacteria and other photosynthetic organisms allowed delineation of the ''photosynthetic gene set'' and demonstrated a significant extent of lateral gene transfer (LGT) among phototrophic bacteria (8)(9)(10)(11). A somewhat surprising result of the latter work has been that genes for most proteins involved in photosynthesis (hereafter ''photosynthetic genes'') were not in the photosynthetic gene set.…”

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confidence: 99%

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The cyanobacterial genome core and the origin of photosynthesis

Mulkidjanian

Koonin

Makarova

et al. 2006

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

291

262

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Comparative analysis of 15 complete cyanobacterial genome sequences, including ''near minimal'' genomes of five strains of Prochlorococcus spp., revealed 1,054 protein families [core cyanobacterial clusters of orthologous groups of proteins (core CyOGs)] encoded in at least 14 of them. The majority of the core CyOGs are involved in central cellular functions that are shared with other bacteria; 50 core CyOGs are specific for cyanobacteria, whereas 84 are exclusively shared by cyanobacteria and plants and͞or other plastid-carrying eukaryotes, such as diatoms or apicomplexans. The latter group includes 35 families of uncharacterized proteins, which could also be involved in photosynthesis. Only a few components of cyanobacterial photosynthetic machinery are represented in the genomes of the anoxygenic phototrophic bacteria Chlorobium tepidum, Rhodopseudomonas palustris, Chloroflexus aurantiacus, or Heliobacillus mobilis. These observations, coupled with recent geological data on the properties of the ancient phototrophs, suggest that photosynthesis originated in the cyanobacterial lineage under the selective pressures of UV light and depletion of electron donors. We propose that the first phototrophs were anaerobic ancestors of cyanobacteria (''procyanobacteria'') that conducted anoxygenic photosynthesis using a photosystem I-like reaction center, somewhat similar to the heterocysts of modern filamentous cyanobacteria. From procyanobacteria, photosynthesis spread to other phyla by way of lateral gene transfer.cyanobacteria ͉ protein families ͉ lateral gene transfer

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Section: Evolution Of Photosynthesis and Lateral Gene Transfermentioning

confidence: 69%

mentioning

confidence: 99%

mentioning

confidence: 99%

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The cyanobacterial genome core and the origin of photosynthesis

Mulkidjanian

Koonin

Makarova

et al. 2006

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

291

262

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“…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: 92%

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.

103

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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

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“…Later work by Raymond and coworkers establishes that horizontal gene transfer has played a major role in the evolutionary development of photosynthesis (Raymond et al 2002).…”

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confidence: 99%