skip to main content
DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

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

Abstract

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. Thesemore » 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:
; ORCiD logo;
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:
Published Article
Journal Name:
Proceedings of the National Academy of Sciences of the United States of America
Additional Journal Information:
Journal Name: Proceedings of the National Academy of Sciences of the United States of America Journal Volume: 114 Journal Issue: 40; Journal ID: ISSN 0027-8424
Publisher:
Proceedings of the National Academy of Sciences
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 = {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. 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 = {2017},
month = {9}
}

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

Citation Metrics:
Cited by: 6 works
Citation information provided by
Web of Science

Save / Share:

Works referenced in this record:

Crown group Oxyphotobacteria postdate the rise of oxygen
journal, July 2016

  • Shih, P. M.; Hemp, J.; Ward, L. M.
  • Geobiology, Vol. 15, Issue 1
  • DOI: 10.1111/gbi.12200

Function, Structure, and Evolution of the RubisCO-Like Proteins and Their RubisCO Homologs
journal, December 2007

  • Tabita, F. R.; Hanson, T. E.; Li, H.
  • Microbiology and Molecular Biology Reviews, Vol. 71, Issue 4
  • DOI: 10.1128/MMBR.00015-07

Support for the Lunar Cataclysm Hypothesis from Lunar Meteorite Impact Melt Ages
journal, December 2000


RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies
journal, January 2014


Molecular Evidence for the Early Evolution of Photosynthesis
journal, September 2000


U-rich Archaean sea-floor sediments from Greenland – indications of >3700 Ma oxygenic photosynthesis
journal, January 2004


Whole-Genome Analysis of Photosynthetic Prokaryotes
journal, November 2002


Photosynthesis and early Earth
journal, October 2015


Origin and early evolution of photosynthesis
journal, August 1992

  • Blankenship, Robert E.
  • Photosynthesis Research, Vol. 33, Issue 2
  • DOI: 10.1007/BF00039173

An uncorrelated relaxed-clock analysis suggests an earlier origin for flowering plants
journal, March 2010

  • Smith, S. A.; Beaulieu, J. M.; Donoghue, M. J.
  • Proceedings of the National Academy of Sciences, Vol. 107, Issue 13
  • DOI: 10.1073/pnas.1001225107

How did LUCA make a living? Chemiosmosis in the origin of life
journal, January 2010


Primary endosymbiosis events date to the later Proterozoic with cross-calibrated phylogenetic dating of duplicated ATPase proteins
journal, June 2013

  • Shih, P. M.; Matzke, N. J.
  • Proceedings of the National Academy of Sciences, Vol. 110, Issue 30
  • DOI: 10.1073/pnas.1305813110

Functional type 2 photosynthetic reaction centers found in the rare bacterial phylum Gemmatimonadetes
journal, May 2014

  • Zeng, Y.; Feng, F.; Medova, H.
  • Proceedings of the National Academy of Sciences, Vol. 111, Issue 21
  • DOI: 10.1073/pnas.1400295111

Examining Archean methanotrophy
journal, May 2016


BLAST+: architecture and applications
journal, January 2009

  • Camacho, Christiam; Coulouris, George; Avagyan, Vahram
  • BMC Bioinformatics, Vol. 10, Issue 1
  • DOI: 10.1186/1471-2105-10-421

Community ecology of hot spring cyanobacterial mats: predominant populations and their functional potential
journal, June 2011

  • Klatt, Christian G.; Wood, Jason M.; Rusch, Douglas B.
  • The ISME Journal, Vol. 5, Issue 8
  • DOI: 10.1038/ismej.2011.73

Temporal metatranscriptomic patterning in phototrophic Chloroflexi inhabiting a microbial mat in a geothermal spring
journal, April 2013

  • Klatt, Christian G.; Liu, Zhenfeng; Ludwig, Marcus
  • The ISME Journal, Vol. 7, Issue 9
  • DOI: 10.1038/ismej.2013.52

Biomarker evidence for green and purple sulphur bacteria in a stratified Palaeoproterozoic sea
journal, October 2005

  • Brocks, Jochen J.; Love, Gordon D.; Summons, Roger E.
  • Nature, Vol. 437, Issue 7060
  • DOI: 10.1038/nature04068

Fractionation of Carbon and Hydrogen Isotopes in Biosynthetic Processes
journal, January 2001

  • Hayes, J. M.
  • Reviews in Mineralogy and Geochemistry, Vol. 43, Issue 1, p. 225-277
  • DOI: 10.2138/gsrmg.43.1.225

Identifying the missing steps of the autotrophic 3-hydroxypropionate CO2 fixation cycle in Chloroflexus aurantiacus
journal, December 2009

  • Zarzycki, Jan; Brecht, Volker; Müller, Michael
  • Proceedings of the National Academy of Sciences, Vol. 106, Issue 50, p. 21317-21322
  • DOI: 10.1073/pnas.0908356106

Chloroflexus aurantiacus secretes 3-hydroxypropionate, a possible intermediate in the assimilation of CO2 and acetate
journal, February 1989

  • Holo, Helge
  • Archives of Microbiology, Vol. 151, Issue 3, p. 252-256
  • DOI: 10.1007/BF00413138

Autotrophic carbon fixation in archaea
journal, May 2010

  • Berg, Ivan A.; Kockelkorn, Daniel; Ramos-Vera, W. Hugo
  • Nature Reviews Microbiology, Vol. 8, Issue 6, p. 447-460
  • DOI: 10.1038/nrmicro2365

MAFFT version 5: improvement in accuracy of multiple sequence alignment
journal, January 2005


A phototrophic gliding filamentous bacterium of hot springs, Chloroflexus aurantiacus, gen. and sp. nov.
journal, January 1974

  • Pierson, Beverly K.; Castenholz, Richard W.
  • Archives of Microbiology, Vol. 100, Issue 1
  • DOI: 10.1007/BF00446302

ProtTest: selection of best-fit models of protein evolution
journal, January 2005


Regular Spliceosomal Introns Are Invasive in Chlamydomonas reinhardtii: 15 Introns in the Recently Relocated Mitochondrial cox2 and cox3 Genes
journal, October 2001

  • Watanabe, Kazuo I.; Ohama, Takeshi
  • Journal of Molecular Evolution, Vol. 53, Issue 4-5
  • DOI: 10.1007/s002390010223

Evolution of Oxygenic Photosynthesis
journal, June 2016


Gene Trees in Species Trees
journal, September 1997


Introduction of a Synthetic CO 2 -fixing Photorespiratory Bypass into a Cyanobacterium
journal, February 2014

  • Shih, Patrick M.; Zarzycki, Jan; Niyogi, Krishna K.
  • Journal of Biological Chemistry, Vol. 289, Issue 14
  • DOI: 10.1074/jbc.C113.543132

Conservation of Distantly Related Membrane Proteins: Photosynthetic Reaction Centers Share a Common Structural Core
journal, August 2006

  • Sadekar, Sumedha; Raymond, Jason; Blankenship, Robert E.
  • Molecular Biology and Evolution, Vol. 23, Issue 11
  • DOI: 10.1093/molbev/msl079

BEAST: Bayesian evolutionary analysis by sampling trees
journal, January 2007


Coassimilation of Organic Substrates via the Autotrophic 3-Hydroxypropionate Bi-Cycle in Chloroflexus aurantiacus
journal, July 2011

  • Zarzycki, Jan; Fuchs, Georg
  • Applied and Environmental Microbiology, Vol. 77, Issue 17, p. 6181-6188
  • DOI: 10.1128/AEM.00705-11

The physiology and habitat of the last universal common ancestor
journal, July 2016


    Works referencing / citing this record:

    On the Origin of Isoprenoid Biosynthesis
    journal, June 2018

    • Hoshino, Yosuke; Gaucher, Eric A.
    • Molecular Biology and Evolution, Vol. 35, Issue 9
    • DOI: 10.1093/molbev/msy120

    Evolutionary Implications of Anoxygenic Phototrophy in the Bacterial Phylum Candidatus Eremiobacterota (WPS-2)
    journal, July 2019

    • Ward, Lewis M.; Cardona, Tanai; Holland-Moritz, Hannah
    • Frontiers in Microbiology, Vol. 10
    • DOI: 10.3389/fmicb.2019.01658