Photoferrotrophy and phototrophic extracellular electron uptake is common in the marine anoxygenic phototroph Rhodovulum sulfidophilum

Gupta, Dinesh; Guzman, Michael S.; Rengasamy, Karthikeyan; Stoica, Andreea; Singh, Rajesh; Ranaivoarisoa, Tahina Onina; Davenport, Emily J.; Bai, Wei; McGinley, Beau; Meacham, J. Mark; Bose, Arpita

doi:10.1038/s41396-021-01015-8

Photoferrotrophy and phototrophic extracellular electron uptake is common in the marine anoxygenic phototroph Rhodovulum sulfidophilum

Journal Article · Sun May 30 00:00:00 EDT 2021 · The ISME Journal

DOI:https://doi.org/10.1038/s41396-021-01015-8· OSTI ID:1785925

^[1]; Guzman, Michael S. ^[2]; Rengasamy, Karthikeyan ^[3]; Stoica, Andreea ^[3]; Singh, Rajesh ^[3]; Ranaivoarisoa, Tahina Onina ^[3]; Davenport, Emily J. ^[3]; Bai, Wei ^[3]; McGinley, Beau ^[3]; ^[4]; ^[3]

Washington Univ., St. Louis, MO (United States); Univ. of California, Berkeley, CA (United States)
Washington Univ., St. Louis, MO (United States); Lawrence Livermore National Lab. (LLNL), Livermore, CA (United States)
Washington Univ., St. Louis, MO (United States)
Washington Univ., St. Louis, MO (United States); Washington Univ., St. Louis, MO (United States). The Inst. of Materials Science and Engineering

Photoferrotrophy allows anoxygenic phototrophs to use reduced iron as an electron donor for primary productivity. Recent work shows that freshwater photoferrotrophs can use electrons from solid-phase conductive substances via phototrophic extracellular electron uptake (pEEU), and the two processes share the underlying electron uptake mechanism. However, the ability of marine phototrophs to perform photoferrotrophy and pEEU, and the contribution of these processes to primary productivity is largely unknown. To fill this knowledge gap, we isolated 15 new strains of the marine anoxygenic phototroph Rhodovulum sulfidophilum on electron donors such as acetate and thiosulfate. We observed that all of the R. sulfidophilum strains isolated can perform photoferrotrophy. Furthermore, we chose strain AB26 as a representative strain to study further, and find that it can also perform pEEU from poised electrodes. We show that during pEEU, AB26 transfers electrons to the photosynthetic electron transport chain. Furthermore, systems biology-guided mutant analysis shows that R. sulfidophilum AB26 uses a previously unknown diheme cytochrome c protein, which we call EeuP, for pEEU but not photoferrotrophy. Homologs of EeuP occur in a range of widely distributed marine microbes. Overall, these results suggest that photoferrotrophy and pEEU contribute to the biogeochemical cycling of iron and carbon in marine ecosystems.

View Accepted Manuscript (DOE)

Research Organization:: Lawrence Livermore National Laboratory (LLNL), Livermore, CA (United States)

Sponsoring Organization:: USDOE National Nuclear Security Administration (NNSA); David and Lucile Packard Foundation; US Army Research Office (ARO); National Science Foundation (NSF); National Institutes of Health (NIH)

Grant/Contract Number:: AC52-07NA27344; SC0014613

OSTI ID:: 1785925

Report Number(s):: LLNL-JRNL--821835; 1033888

Journal Information:: The ISME Journal, Journal Name: The ISME Journal Vol. 15; ISSN 1751-7362

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

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