Introduction of a Synthetic CO2-fixing Photorespiratory Bypass into a Cyanobacterium

Shih, Patrick M.; Zarzycki, Jan; Niyogi, Krishna; Kerfeld, Cheryl A.

doi:10.1074/jbc.c113.543132

Cited by 91 publications

(66 citation statements)

References 30 publications

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“…It additionally suggests that, although the 3HP bicycle is both energetically efficient and insensitive to dioxygen-features that make it unique from all other carbon fixation pathways-one of the reasons it was never used for oxygenic photosynthesis may have been because it wasn't present during the radiation of Cyanobacteria and the emergence of plastids. If correct, efforts to build a synthetic 3HP bicycle into oxygenic photosynthetic organisms might yield valuable solutions to the large carbon losses incurred by photorespiration (33).…”

Section: Resultsmentioning

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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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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Section: Resultsmentioning

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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103

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“…The hypothetical C4/glyoxylate cycle (41) may be easier to implement because it requires only four enzymes, although a pathway to convert glyoxylate, the product of this cycle, into a metabolically useful intermediate would also be required. In fact, the second cycle of the recently demonstrated 3-hydroxypropionate bicycle produces a metabolically useful product by converting glycolate to pyruvate (38). Another exciting approach would be to design a completely orthogonal pathway involving intermediates that are not shared by any existing pathway in the organism.…”

Section: Targets Of Opportunitymentioning

confidence: 99%

“…Among them, the conversion of glycolate into glycerate via glyoxylate and tartronic semialdehyde can increase leaf photosynthetic CO 2 uptake due to both the decreased energy demand of photorespiration and increased CO 2 concentration in chloroplasts (36). Another promising experimental strategy is to introduce new anaplerotic pathways to recycle glycolate without an associated CO 2 loss, such as the 3-hydroxypropionate pathway that converts glyoxylate to pyruvate in some bacteria (37,38). It might also be possible to design entirely novel pathways, including the hypothetical one shown in Fig.…”

Section: Targets Of Opportunitymentioning

confidence: 99%

Redesigning photosynthesis to sustainably meet global food and bioenergy demand

Ort

Merchant

Alric

et al. 2015

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

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817

628

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The world's crop productivity is stagnating whereas population growth, rising affluence, and mandates for biofuels put increasing demands on agriculture. Meanwhile, demand for increasing cropland competes with equally crucial global sustainability and environmental protection needs. Addressing this looming agricultural crisis will be one of our greatest scientific challenges in the coming decades, and success will require substantial improvements at many levels. We assert that increasing the efficiency and productivity of photosynthesis in crop plants will be essential if this grand challenge is to be met. Here, we explore an array of prospective redesigns of plant systems at various scales, all aimed at increasing crop yields through improved photosynthetic efficiency and performance. Prospects range from straightforward alterations, already supported by preliminary evidence of feasibility, to substantial redesigns that are currently only conceptual, but that may be enabled by new developments in synthetic biology. Although some proposed redesigns are certain to face obstacles that will require alternate routes, the efforts should lead to new discoveries and technical advances with important impacts on the global problem of crop productivity and bioenergy production.light capture/conversion | carbon capture/conversion | smart canopy | enabling plant biotechnology tools | sustainable crop production Increasing demands for global food production over the next several decades portend a huge burden on the world's shrinking farmlands. Increasing global affluence, population growth, and demands for a bioeconomy (including livestock feed, bioenergy, chemical feedstocks, and biopharmaceuticals) will all require increased agricultural productivity, perhaps by as much as 60-120% over 2005 levels (e.g., refs. 1 and 2), putting increased productivity on a collision course with environmental and sustainability goals (3). The 45 y from 1960 to 2005 saw global food production grow ∼160%, mostly (135%) by improved production on

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“…Parikh et al ., 2006; Durão et al ., 2015), introducing more efficient photorespiration pathways (e.g. Shih et al ., 2014) and introducing CO 2 concentrating mechanisms to increase the carboxylating activity of RubisCO (e.g. Bonacci et al ., 2012; Kamennaya et al ., 2015).…”

mentioning

confidence: 99%

A warm welcome for alternative CO₂ fixation pathways in microbial biotechnology

Claassens

2016

Microbial Biotechnology

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Introduction of a Synthetic CO2-fixing Photorespiratory Bypass into a Cyanobacterium

Cited by 91 publications

References 30 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

Redesigning photosynthesis to sustainably meet global food and bioenergy demand

A warm welcome for alternative CO₂ fixation pathways in microbial biotechnology

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Introduction of a Synthetic CO2-fixing Photorespiratory Bypass into a Cyanobacterium

Cited by 91 publications

References 30 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

Redesigning photosynthesis to sustainably meet global food and bioenergy demand

A warm welcome for alternative CO2 fixation pathways in microbial biotechnology

Contact Info

Product

Resources

About

A warm welcome for alternative CO₂ fixation pathways in microbial biotechnology