title: Syntrophic anaerobic photosynthesis via direct interspecies electron transfer.
abstract: 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. This process could be exploited for biotechnological applications, such as waste treatment and bioenergy production, using engineered phototrophic microbial communities.
authors.affiliation: The Gene and Linda Voiland School of Chemical Engineering and Bioengineering, Washington State University, Pullman, Washington 99164, USA.
authors.forename: Phuc T
authors.initials: PT
authors.lastname: Ha
authors.affiliation: Biological Sciences Division, Pacific Northwest National Laboratory, Richland, Washington 99354, USA.
authors.forename: Stephen R
authors.initials: SR
authors.lastname: Lindemann
authors.affiliation: Department of Biological Sciences and Technology, School of Environmental Studies, China University of Geoscience, Wuhan, Hubei 430074, China.
authors.forename: Liang
authors.initials: L
authors.lastname: Shi
authors.affiliation: Environmental Molecular Sciences Laboratory, Pacific Northwest National Laboratory, Richland, Washington 99354, USA.
authors.forename: Alice C
authors.initials: AC
authors.lastname: Dohnalkova
authors.affiliation: Biological Sciences Division, Pacific Northwest National Laboratory, Richland, Washington 99354, USA.
authors.forename: James K
authors.initials: JK
authors.lastname: Fredrickson
authors.affiliation: Department of Microbiology, Southern Illinois University, Carbondale, Illinois 62901, USA.
authors.forename: Michael T
authors.initials: MT
authors.lastname: Madigan
authors.affiliation: The Gene and Linda Voiland School of Chemical Engineering and Bioengineering, Washington State University, Pullman, Washington 99164, USA.
authors.forename: Haluk
authors.initials: H
authors.lastname: Beyenal
mesh_terms: D000693:Anaerobiosis / Q000502:physiology*; D052818:Autotrophic Processes / Q000502:physiology; D056804:Biofuels; D002244:Carbon / Q000378:metabolism*; D019414:Chlorobi / Q000254:growth & development / Q000378:metabolism* / Q000648:ultrastructure; D018920:Coculture Techniques; D003580:Cytochromes / Q000378:metabolism; D004583:Electrons; D045302:Geobacter / Q000254:growth & development / Q000378:metabolism* / Q000648:ultrastructure; D010084:Oxidation-Reduction; D010788:Photosynthesis / Q000502:physiology*; D018272:Porins / Q000378:metabolism
chemical_list: D056804:Biofuels; D003580:Cytochromes; D018272:Porins; D002244:Carbon