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.

Ecology and evolution of metabolic cross-feeding interactions in bacteria

“…143 or (F) intercellular nanotubes that allow an exchange of cytoplasmic contents. 145,147 Moreover, also (G) flagella-like structures 67,148 or (H) a direct surface contact 149,150 can facilitate the exchange of metabolites between cells. of outer membrane material (i.e.…”

Syntrophus conductive pili demonstrate that common hydrogen-donating syntrophs can have a direct electron transfer option

“…It has previously been considered that DIET is primarily restricted to environments in which Geobacter species are abundant [8][9][10][11][12] , because Geobacter species are the only microbes in pure culture that have been definitively shown to function as electron-donating partners for DIET 9,[13][14][15][16][17] . Studies with Geobacter metallireducens have suggested that electrically conductive pili (e-pili) are an important conduit for electron transfer from the electron-donating partner 9,14,17,18 .…”

Syntrophic growth with direct interspecies electron transfer between pili-free Geobacter species

“…(ii) DIET has been proposed to control methane release [4][5][6]. (iii) A recent finding indicates that DIET can be electron sources to support anaerobic photosynthesis [7].…”

“…The proposed mechanism of DIET for these defined Geobacter species cocultures is that conductive pili from both Geobacter species facilitate the interspecific transfer of electrons with the help of cytochromes, which emphasizes the importance of the high conductivity of pili during DIET [9]. The importance of cytochromes in DIET is clear, such as the following: (i) the mutation of the abovementioned cytochromes inhibits the formation of cocultures; (ii) the DIET community, such as anaerobic bioreactors for treatment of brewery wastes [10], methanogenic digestion of wastewater [3] and rice paddy soils [11], always contains Geobacter species at high abundance, which take a hall-mark feature of abundance with c-type cytochromes [12]; (iii) The metagenome of proposed DIET-based consortia of anaerobic methane-oxidizing archaeal group 1 (ANME-1) methanotrophic archaea coupled to sulfate reduction contains abundant genes encoding multi-heme cytochromes [13]; (iv) in the DIET consortia of ANME-2 with its sulfate-reducing partner, regions with dense heme-staining in the multicellular assemblages are visualized indicating a cytochrome-based electron transfer between species [5]; and (v) the outer membrane surface cytochrome OmcB of G. sulfurreducens is necessary for syntrophic anaerobic photosynthesis [7].…”