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Biophotoelectrochemical process co-driven by dead microalgae and live bacteria

The ISME Journal volume 17, pages 712–719 (2023)Cite this article

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Abstract

Anaerobic reduction processes in natural waters can be promoted by dead microalgae that have been attributed to nutrient substances provided by the decomposition of dead microalgae for other microorganisms. However, previous reports have not considered that dead microalgae may also serve as photosensitizers to drive microbial reduction processes. Here we demonstrate a photoelectric synergistic linkage between dead microalgae and bacteria capable of extracellular electron transfer (EET). Illumination of dead Raphidocelis subcapitata resulted in two-fold increase in the rate of anaerobic bioreduction by pure Geobacter sulfurreducens, suggesting that photoelectrons generated from the illuminated dead microalgae were transferred to the EET-capable microorganisms. Similar phenomena were observed in NO3− reduction driven by irradiated dead Chlorella vulgaris and living Shewanella oneidensis, and Cr(VI) reduction driven by irradiated dead Raphidocelis subcapitata and living Bacillus subtilis. Enhancement of bioreduction was also seen when the killed microalgae were illuminated in mixed-culture lake water, suggesting that EET-capable bacteria were naturally present and this phenomenon is common in post-bloom systems. The intracellular ferredoxin-NADP+-reductase is inactivated in the dead microalgae, allowing the production and extracellular transfer of photoelectrons. The use of mutant strains confirmed that the electron transport pathway requires multiheme cytochromes. Taken together, these results suggest a heretofore overlooked biophotoelectrochemical process jointly mediated by illumination of dead microalgae and live EET-capable bacteria in natural ecosystems, which may add an important component in the energetics of bioreduction phenomena particularly in microalgae-enriched environments.

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Fig. 1: Anaerobic reduction process co-driven by dead Raphidocelis subcapitata and live Geobacter sulfurreducens.
Fig. 2: Photoelectric mechanisms in the dead Raphidocelis subcapitata–live Geobacter sulfurreducens experiment.
Fig. 3: Anaerobic reduction process co-driven by dead microalgae and live mixed-bacteria in lake water.
Fig. 4: Evidences for a biophotoelectrochemical process in a mixed-bacteria environment.
Fig. 5: Proposed photoelectric mechanism of the anaerobic reduction process co-driven by dead microalgae and live bacteria.

Data availability

The DNA sequence raw data have been deposited in the NCBI Sequence Read Archive (http://www.ncbi.nlm.nih.gov/sra) with the accession numbers SRR23217474-SRR23217485 under the BioProject PRJNA925680. All other data are available at Zenodo (https://doi.org/10.5281/zenodo.7553088).

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Acknowledgements

This work was financially supported by the National Natural Science Foundation of China (92251301 and 42277101), and the Program for Guangdong Introducing Innovative and Entrepreneurial Teams (2019ZT08L213).

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Authors and Affiliations

  1. Guangdong Provincial Key Laboratory of Water Quality Improvement and Ecological Restoration for Watersheds, School of Ecology, Environment and Resources, Guangdong University of Technology, Guangzhou, China

    Shanshan Chen, Lanlan Zhang, Yuting Yang & Tiangang Luan

  2. Fujian Provincial Key Laboratory of Soil Environmental Health and Regulation, College of Resources and Environment, Fujian Agriculture and Forestry University, Fuzhou, China

    Jin Chen, Shaofu Huang, Xing Liu, Shungui Zhou & Christopher Rensing

  3. Department of Earth Science, University of Southern California, Los Angeles, CA, USA

    Kenneth H. Nealson

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  1. Shanshan Chen
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Contributions

SC designed the experiments, conducted analyses and wrote the first draft of the manuscript. JC, LZ, and YY performed the experiments, collected the data and drew figures. SH and XL interpreted the data. TL and SZ supervised the experiments. SZ, KHN and CR revised the manuscript. All authors read, revised and approved the final manuscript.

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Correspondence to Shungui Zhou.

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Chen, S., Chen, J., Zhang, L. et al. Biophotoelectrochemical process co-driven by dead microalgae and live bacteria. ISME J 17, 712–719 (2023). https://doi.org/10.1038/s41396-023-01383-3

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