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Title: Syntrophic anaerobic photosynthesis via direct interspecies electron transfer

Microbial phototrophs, key primary producers on Earth, use H 2O, H 2, H 2S and other reduced inorganic compounds as electron donors. Here we describe a form of metabolism linking anoxygenic photosynthesis to anaerobic respiration that we call ‘syntrophic anaerobic photosynthesis’. We show that photoautotrophy in the green sulfur bacterium Prosthecochloris aestaurii can be driven by either electrons from a solid electrode or acetate oxidation via direct interspecies electron transfer from a heterotrophic partner bacterium, Geobacter sulfurreducens. Photosynthetic growth of P. aestuarii using reductant provided by either an electrode or syntrophy is robust and light-dependent. In contrast, P. aestuarii does not grow in co-culture with a G. sulfurreducens mutant lacking a trans-outer membrane porin-cytochrome protein complex required for direct intercellular electron transfer. Syntrophic anaerobic photosynthesis is therefore a carbon cycling process that could take place in anoxic environments. Lastly, this process could be exploited for biotechnological applications, such as waste treatment and bioenergy production, using engineered phototrophic microbial communities.
Authors:
 [1] ;  [2] ;  [3] ;  [2] ;  [2] ;  [4] ;  [1]
  1. Washington State Univ., Pullman, WA (United States)
  2. Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
  3. China Univ. of Geoscience, Hubei (China)
  4. Southern Illinois Univ., Carbondale, IL (United States)
Publication Date:
Report Number(s):
PNNL-SA-119245
Journal ID: ISSN 2041-1723; 48418; KP1601010
Grant/Contract Number:
AC05-76RL01830
Type:
Accepted Manuscript
Journal Name:
Nature Communications
Additional Journal Information:
Journal Volume: 8; Journal ID: ISSN 2041-1723
Publisher:
Nature Publishing Group
Research Org:
Pacific Northwest National Lab. (PNNL), Richland, WA (United States). Environmental Molecular Sciences Lab. (EMSL)
Sponsoring Org:
USDOE
Country of Publication:
United States
Language:
English
Subject:
54 ENVIRONMENTAL SCIENCES; 59 BASIC BIOLOGICAL SCIENCES; Environmental Molecular Sciences Laboratory; bacterial physiology; environmental microbiology; symbiosis
OSTI Identifier:
1347843

Ha, Phuc T., Lindemann, Stephen R., Shi, Liang, Dohnalkova, Alice C., Fredrickson, James K., Madigan, Michael T., and Beyenal, Haluk. Syntrophic anaerobic photosynthesis via direct interspecies electron transfer. United States: N. p., Web. doi:10.1038/ncomms13924.
Ha, Phuc T., Lindemann, Stephen R., Shi, Liang, Dohnalkova, Alice C., Fredrickson, James K., Madigan, Michael T., & Beyenal, Haluk. Syntrophic anaerobic photosynthesis via direct interspecies electron transfer. United States. doi:10.1038/ncomms13924.
Ha, Phuc T., Lindemann, Stephen R., Shi, Liang, Dohnalkova, Alice C., Fredrickson, James K., Madigan, Michael T., and Beyenal, Haluk. 2017. "Syntrophic anaerobic photosynthesis via direct interspecies electron transfer". United States. doi:10.1038/ncomms13924. https://www.osti.gov/servlets/purl/1347843.
@article{osti_1347843,
title = {Syntrophic anaerobic photosynthesis via direct interspecies electron transfer},
author = {Ha, Phuc T. and Lindemann, Stephen R. and Shi, Liang and Dohnalkova, Alice C. and Fredrickson, James K. and Madigan, Michael T. and Beyenal, Haluk},
abstractNote = {Microbial phototrophs, key primary producers on Earth, use H2O, H2, H2S and other reduced inorganic compounds as electron donors. Here we describe a form of metabolism linking anoxygenic photosynthesis to anaerobic respiration that we call ‘syntrophic anaerobic photosynthesis’. We show that photoautotrophy in the green sulfur bacterium Prosthecochloris aestaurii can be driven by either electrons from a solid electrode or acetate oxidation via direct interspecies electron transfer from a heterotrophic partner bacterium, Geobacter sulfurreducens. Photosynthetic growth of P. aestuarii using reductant provided by either an electrode or syntrophy is robust and light-dependent. In contrast, P. aestuarii does not grow in co-culture with a G. sulfurreducens mutant lacking a trans-outer membrane porin-cytochrome protein complex required for direct intercellular electron transfer. Syntrophic anaerobic photosynthesis is therefore a carbon cycling process that could take place in anoxic environments. Lastly, this process could be exploited for biotechnological applications, such as waste treatment and bioenergy production, using engineered phototrophic microbial communities.},
doi = {10.1038/ncomms13924},
journal = {Nature Communications},
number = ,
volume = 8,
place = {United States},
year = {2017},
month = {1}
}