Photosynthetic hydrogen production by droplet-based microbial micro-reactors under aerobic conditions

Zhijun Xu,Xiaoman Liu,Lei Wang,Xin Huang,Stephen Mann,Shangsong Li,Mei Li,Shengliang Wang,Chunyu Zhao

doi:10.1038/s41467-020-19823-5

Abstract

The spontaneous self-assembly of multicellular ensembles into living materials with synergistic structure and function remains a considerable challenge in biotechnology and synthetic biology. Here, we exploit the aqueous two-phase separation of dextran-in-PEG emulsion micro-droplets for the capture, spatial organization and immobilization of algal cells or algal/bacterial cell communities to produce discrete multicellular spheroids capable of both aerobic (oxygen producing) and hypoxic (hydrogen producing) photosynthesis in daylight under air. We show that localized oxygen depletion results in hydrogen production from the core of the algal microscale reactor, and demonstrate that enhanced levels of hydrogen evolution can be achieved synergistically by spontaneously enclosing the photosynthetic cells within a shell of bacterial cells undergoing aerobic respiration. Our results highlight a promising droplet-based environmentally benign approach to dispersible photosynthetic microbial micro-reactors comprising segregated cellular micro-niches with dual functionality, and provide a step towards photobiological hydrogen production under aerobic conditions.

Highlights

The spontaneous self-assembly of multicellular ensembles into living materials with synergistic structure and function remains a considerable challenge in biotechnology and synthetic biology
We developed a facile strategy for the preparation of populations of discrete microscale microbial reactors with spatially segregated multicellular micro-niches capable of aerobic or hypoxic photosynthesis at room temperature in air
Large numbers of Chlorella algal cells were spontaneously captured within BSA-stabilized w/w dextran-in-PEG emulsion droplets and compacted into closely packed spheroidal aggregates by hyperosmotic shrinkage and in situ formation of a BSA/dextran hydrogel matrix

Summary

Introduction

The spontaneous self-assembly of multicellular ensembles into living materials with synergistic structure and function remains a considerable challenge in biotechnology and synthetic biology. We exploit the aqueous two-phase separation of dextran-in-PEG emulsion micro-droplets for the capture, spatial organization and immobilization of algal cells or algal/ bacterial cell communities to produce discrete multicellular spheroids capable of both aerobic (oxygen producing) and hypoxic (hydrogen producing) photosynthesis in daylight under air. Given that the renewable and biological production of hydrogen from solar energy is attracting considerable interest, in this study, we exploit the aqueous two-phase separation of dextran-in PEG emulsion droplets for the capture, spatial organization and immobilization of living algal cells to produce dispersible microscale microbial reactors capable of both aerobic and hypoxic photosynthesis in daylight under air (Fig. 1a–c). Our methodology offers a proof-ofprinciple for utilizing aqueous two-phase separated droplets as vectors for controlling algal cell organization and photosynthesis in synthetic micro-spaces and provides a step towards the bottomup assembly of photobiological micro-reactors with multiple functionalities

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Results

Conclusion