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

The ISME Journal volume 15, pages 3384–3398 (2021)Cite this article

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Abstract

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. 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.

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Fig. 1: AB26 is a metabolically versatile phototrophic Fe(II)-oxidizing bacterium.
Fig. 2: AB26 grows by photoferrotrophy.
Fig. 3: AB26 performs phototrophic extracellular electron uptake.
Fig. 4: Photosynthetic electron transfer is required for extracellular electron uptake.
Fig. 5: Expression analysis of carbon fixation and storage pathways.
Fig. 6: Cytochrome c proteins are upregulated under photoferrotrophy and pEEU.
Fig. 7: Diheme cytochrome c is important for phototrophic extracellular electron uptake by AB26.

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Acknowledgements

The authors acknowledge Prof. Robert Kranz [Washington University in St. Louis (WUSTL)] for valuable assistance with heme protein characterization. We thank the Washington University’s Genome Technology and Access Center (GTAC) for technical guidance and transcriptome sequencing. The authors thank the Institute of Materials Science and Engineering at Washington University in St. Louis, which provided facilities, resources, and assistance in microfabrication. We thank Bradley Evans and Shin-Cheng Tzeng from Proteomics and Mass Spectrometry facility, DDPSC. This work was supported by the following grants to AB: The David and Lucile Packard Foundation Fellowship (201563111), the U.S. Department of Energy (grant number DESC0014613), and the U.S. Department of Defense, Army Research Office (grant number W911NF-18-1-0037). Gordon and Betty Moore Foundation, National Science Foundation (Grant Number 2021822), and the U.S. Department of Energy by Lawrence Livermore National Laboratory under Contract DEAC5207NA27344 (LLNL-JRNL-812309), and AB was also funded by a Collaboration Initiation Grant, an Office of the Vice-Chancellor of Research Grant, and an International Center for Energy, Environment, and Sustainability Grant from Washington University in St. Louis. EJD is supported by an Institutional Training Grant in Genomic Science from the NIH (T32 HG000045-18). MSG was supported by the Initiative for Maximizing Student Development (IMSD) training grant from the U.S. National Institutes of Health (grant number R25-GM103757). This work was performed under the auspices of the U.S. Department of Energy by Lawrence Livermore National Laboratory under Contract DE-AC52-07NA27344 (LLNL-JRNL-821835).

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Author notes

  1. Dinesh Gupta

    Present address: Department of Molecular and Cell Biology, University of California, Berkeley, CA, USA

  2. Michael S. Guzman

    Present address: Biosciences and Biotechnology Division, Physical and Life Sciences Directorate, Lawrence Livermore National Laboratory, Livermore, CA, USA

  3. These authors contributed equally: Dinesh Gupta, Michael S. Guzman, Karthikeyan Rengasamy.

Authors and Affiliations

  1. Department of Biology, Washington University in St. Louis, St. Louis, MO, USA

    Dinesh Gupta, Michael S. Guzman, Karthikeyan Rengasamy, Rajesh Singh, Tahina Onina Ranaivoarisoa, Emily J. Davenport, Beau McGinley & Arpita Bose

  2. Department of Mechanical Engineering and Materials Science, Washington University in St. Louis, St. Louis, MO, USA

    Andreea Stoica & J. Mark Meacham

  3. Department of Energy, Environmental and Chemical Engineering, Washington University in St. Louis, St. Louis, MO, USA

    Wei Bai

  4. The Institute of Materials Science and Engineering, Washington University in St. Louis, St. Louis, MO, USA

    J. Mark Meacham

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Contributions

DG, MSG, KR, RS, EJD, and AB designed the research. AS, KR, and JMM designed, fabricated, and operated the µ-BEC arrays. DG, MSG, KR, TOR, RS, WB, and BM collected the data. DG, MSG, KR, TOR, RS, EJD, and AB analyzed and interpreted the data. DG, MSG, KR, RS, and AB wrote the manuscript with contributions from other authors. All authors reviewed, revised, and approved the final manuscript.

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Correspondence to Arpita Bose.

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Gupta, D., Guzman, M.S., Rengasamy, K. et al. Photoferrotrophy and phototrophic extracellular electron uptake is common in the marine anoxygenic phototroph Rhodovulum sulfidophilum. ISME J 15, 3384–3398 (2021). https://doi.org/10.1038/s41396-021-01015-8

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