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

Abstract

We report 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 bicycle—evolved 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.more » Finally, 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.« less

Authors:
 [1]; ORCiD logo [2];  [2]
  1. Joint BioEnergy Institute, Emeryville, CA (United States). Feedstocks Division; Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Environmental Genomics and Systems Biology Division
  2. California Inst. of Technology (CalTech), Pasadena, CA (United States). Division of Geological and Planetary Sciences
Publication Date:
Research Org.:
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23)
OSTI Identifier:
1392687
Alternate Identifier(s):
OSTI ID: 1426736
Grant/Contract Number:  
AC02-05CH11231
Resource Type:
Journal Article: Published Article
Journal Name:
Proceedings of the National Academy of Sciences of the United States of America
Additional Journal Information:
Journal Volume: 114; Journal Issue: 40; Journal ID: ISSN 0027-8424
Publisher:
National Academy of Sciences, Washington, DC (United States)
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; 58 GEOSCIENCES; carbon fixation; phototrophy; molecular clock; comparative genomics

Citation Formats

Shih, Patrick M., Ward, Lewis M., and Fischer, Woodward W. Evolution of the 3-hydroxypropionate bicycle and recent transfer of anoxygenic photosynthesis into the Chloroflexi. United States: N. p., 2017. Web. doi:10.1073/pnas.1710798114.
Shih, Patrick M., Ward, Lewis M., & Fischer, Woodward W. Evolution of the 3-hydroxypropionate bicycle and recent transfer of anoxygenic photosynthesis into the Chloroflexi. United States. doi:10.1073/pnas.1710798114.
Shih, Patrick M., Ward, Lewis M., and Fischer, Woodward W. Mon . "Evolution of the 3-hydroxypropionate bicycle and recent transfer of anoxygenic photosynthesis into the Chloroflexi". United States. doi:10.1073/pnas.1710798114.
@article{osti_1392687,
title = {Evolution of the 3-hydroxypropionate bicycle and recent transfer of anoxygenic photosynthesis into the Chloroflexi},
author = {Shih, Patrick M. and Ward, Lewis M. and Fischer, Woodward W.},
abstractNote = {We report 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 bicycle—evolved 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. Finally, 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.},
doi = {10.1073/pnas.1710798114},
journal = {Proceedings of the National Academy of Sciences of the United States of America},
number = 40,
volume = 114,
place = {United States},
year = {Mon Sep 18 00:00:00 EDT 2017},
month = {Mon Sep 18 00:00:00 EDT 2017}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record at 10.1073/pnas.1710798114

Citation Metrics:
Cited by: 2 works
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