A physiological perspective on the origin and evolution of photosynthesis

William F. Martin, Donald Ashley Bryant, J. Thomas Beatty

Research output: Contribution to journalReview article

26 Citations (Scopus)

Abstract

The origin and early evolution of photosynthesis are reviewed from an ecophysiological perspective. Earth's first ecosystems were chemotrophic, fueled by geological H2 at hydrothermal vents and, required flavin-based electron bifurcation to reduce ferredoxin for CO2 fixation. Chlorophyll-based phototrophy (chlorophototrophy) allowed autotrophs to generate reduced ferredoxin without electron bifurcation, providing them access to reductants other than H2. Because high-intensity, short-wavelength electromagnetic radiation at Earth's surface would have been damaging for the first chlorophyll (Chl)-containing cells, photosynthesis probably arose at hydrothermal vents under low-intensity, long-wavelength geothermal light. The first photochemically active pigments were possibly Zn-tetrapyrroles. We suggest that (i) after the evolution of red-absorbing Chl-like pigments, the first light-driven electron transport chains reduced ferredoxin via a type-1 reaction center (RC) progenitor with electrons from H2S; (ii) photothioautotrophy, first with one RC and then with two, was the bridge between H2-dependent chemolithoautotrophy and water-splitting photosynthesis; (iii) photothiotrophy sustained primary production in the photic zone of Archean oceans; (iv) photosynthesis arose in an anoxygenic cyanobacterial progenitor; (v) Chl a is the ancestral Chl; and (vi), anoxygenic chlorophototrophic lineages characterized so far acquired, by horizontal gene transfer, RCs and Chl biosynthesis with or without autotrophy, from the architects of chlorophototrophy-the cyanobacterial lineage.

Original languageEnglish (US)
Pages (from-to)205-231
Number of pages27
JournalFEMS Microbiology Reviews
Volume42
Issue number2
DOIs
StatePublished - Jan 1 2018

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Photosynthesis
Chlorophyll
Ferredoxins
Phototrophic Processes
Hydrothermal Vents
Electrons
Chemoautotrophic Growth
Autotrophic Processes
Tetrapyrroles
Electromagnetic Radiation
Light
Horizontal Gene Transfer
Reducing Agents
Electron Transport
Oceans and Seas
Ecosystem
Water

All Science Journal Classification (ASJC) codes

  • Microbiology
  • Infectious Diseases

Cite this

Martin, William F. ; Bryant, Donald Ashley ; Beatty, J. Thomas. / A physiological perspective on the origin and evolution of photosynthesis. In: FEMS Microbiology Reviews. 2018 ; Vol. 42, No. 2. pp. 205-231.
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A physiological perspective on the origin and evolution of photosynthesis. / Martin, William F.; Bryant, Donald Ashley; Beatty, J. Thomas.

In: FEMS Microbiology Reviews, Vol. 42, No. 2, 01.01.2018, p. 205-231.

Research output: Contribution to journalReview article

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