Horizontal Transfer of the Photosynthesis Gene Cluster and Operon Rearrangement in Purple Bacteria

Igarashi, Naoki; Harada, Jiro; Nagashima, Sakiko; Matsuura, Kiyotaka; Shimada, Keizo; Nagashima, Kenji V. P.

doi:10.1007/s002390010163

Cited by 123 publications

(112 citation statements)

References 39 publications

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“…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.…”

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confidence: 99%

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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.

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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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Section: Resultsmentioning

confidence: 99%

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.

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“…Since Acp. rubrum also has a similar gene cluster for photopigment biosynthesis including bchB, bchD, bchF, bchH, bchI, bchL, bchN, bchP, and a carotenoid biosynthesis gene (crtI) (Masuda et al, 1999), it is likely that Acidiphilium has a large photosynthetic gene cluster as revealed in some purple bacteria (Igarashi et al, 2001).…”

Section: Genes For Photosynthetic Apparatusmentioning

confidence: 96%

Aerobic anoxygenic photosynthetic bacteria with zinc-bacteriochlorophyll.

Hiraishi

Shimada

2001

J. Gen. Appl. Microbiol.

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IntroductionChlorophylls (Chls) and bacteriochlorophylls (BChls) are porphyrin derivatives chelated with magnesium, and represent a class of lipophilic pigments involved in natural photosynthesis. There has been no rational explanation for why extant phototrophic organisms have used Mg exclusively as the central metal with which the chlorophyllous pigments are complexed. Apart from this question, phototrophic organisms that use Chls or BChls containing metals other than Mg were unknown for a long time. Recently, this common understanding of natural photosynthesis was unexpectedly modified by the new finding that a novel purple pigment, zinc-chelated-BChl (Zn-BChl) (for abbreviations, see Takaichi et al. (1999)), was discovered in a specific group of obligately aerobic bacteria (Hiraishi et al., 1998;Wakao et al., 1996Wakao et al., , 1999.It has been satisfactorily demonstrated that BChls are present not only in facultatively and obligately anaerobic anoxygenic phototrophic bacteria but also in large numbers of species of obligately aerobic bacteria Naturally occurring chlorophyllous pigments, which function as the cofactor in the early photochemical reaction of photosynthesis, have been proven beyond question to be magnesium-complexed porphyrin derivatives. Phototrophic organisms that use (bacterio)chlorophylls ([B]Chls)containing metals other than Mg were unknown for a long time. This common knowledge of natural photosynthesis has recently been modified by the striking finding that a novel purple pigment, zinc-chelated-BChl (Zn-BChl) a, is present as the major and functional pigment in species of the genus Acidiphilium. Acidiphilium species are obligately acidophilic chemoorganotrophic bacteria that grow and produce photopigments only under aerobic conditions. Although the mechanism of photosynthesis with Zn-BChl a in Acidiphilium species is similar to that seen in common purple bacteria, some characteristic photosynthetic features of the acidophilic bacteria are also found. The discovery of natural photosynthesis with Zn-BChl has not only provided a new insight into our understanding of bacterial photosynthesis but also raised some interesting questions to be clarified. The major questions are why the acidophilic bacteria have selected ZnBChl for their photosynthesis and how they synthesize Zn-BChl and express photosynthetic activity with it in their natural habitats. In this article we review the current knowledge of the biology of Acidiphilium as aerobic photosynthetic bacteria with Zn-BChl a and discuss the interesting topics noted above.

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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: 99%

The cyanobacterial genome core and the origin of photosynthesis

Mulkidjanian

Koonin

Makarova

et al. 2006

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

288

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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Horizontal Transfer of the Photosynthesis Gene Cluster and Operon Rearrangement in Purple Bacteria

Cited by 123 publications

References 39 publications

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

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

Aerobic anoxygenic photosynthetic bacteria with zinc-bacteriochlorophyll.

The cyanobacterial genome core and the origin of photosynthesis

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