A miniaturized bionic ocean-battery mimicking the structure of marine microbial ecosystems

Article https://doi.org/10.1038/s41467-022-33358-x A miniaturized bionic ocean-battery mimicking the structure of marine microbial ecosystems Received: 1 December 2021 Check for updates 1234567890():,; 1234567890():,; Accepted: 14 September 2022 Huawei Zhu 1,2, Liru Xu1,2, Guodong Luan3, Tao Zhan 4,5, Zepeng Kang4,5, Chunli Li6, Xuefeng Lu 3 , Xueli Zhang 4,5 , Zhiguang Zhu 4,5 , Yanping Zhang 1 & Yin Li 1 Marine microbial ecosystems can be viewed as a huge ocean-battery charged by solar energy. It provides a model for fabricating bio-solar cell, a bioelectrochemical system that converts light into electricity. Here, we fabricate a biosolar cell consisting of a four-species microbial community by mimicking the ecological structure of marine microbial ecosystems. We demonstrate such ecological structure consisting of primary producer, primary degrader, and ultimate consumers is essential for achieving high power density and stability. Furthermore, the four-species microbial community is assembled into a spatial-temporally compacted cell using conductive hydrogel as a sedimentlike anaerobic matrix, forming a miniaturized bionic ocean-battery. This battery directly converts light into electricity with a maximum power of 380 μW and stably operates for over one month. Reproducing the photoelectric conversion function of marine microbial ecosystems in this bionic battery overcomes the sluggish and network-like electron transfer, showing the biotechnological potential of synthetic microbial ecology. The ocean, which covers ~70% of the Earth’s surface, is a huge solar energy converter1. Approximately one-half of the global primary production occurs in the ocean2–4. It is estimated that 90% of marine biomass is microorganisms, which are centrally involved in the energy conversion1,5–7. In marine microbial ecosystems, the primary producers in the euphotic zone of water column such as the cyanobacteria Prochlorococcus and Synechococcus harvest solar energy through photosynthesis, fix carbon dioxide, and release organic matter (Fig. 1a)8,9. Organic matter can be consumed by heterotrophic plankton lived in the water column, or deposited into the marine sediments through sinking and burial10. Marine sediments is a large anaerobic bioreactor where organic matter is slowly degraded and fully oxidized by two types of heterotrophic microorganisms, eventually achieving complete remineralization (Fig. 1a)11. One type are the primary degraders, also known as fermentative microorganisms12,13, which are responsible for anaerobic degradation of complex or high-molecular-weight organic compounds (e.g., polysaccharides and proteins) into smaller organic compounds (e.g., organic acids and amino acids)14. Another type are the ultimate consumers, which are responsible for the complete oxidation of organic compounds into carbon dioxide by respiring alternative electron acceptors, including NO3-, Mn4+, Fe3+ and SO42− (Fig. 1a)15. When all alternative electron acceptors were exhausted, methanogenesis by archaea becomes an important process for organic matter decomposition in deep sediments16. Through photosynthetic 1 CAS Key Laboratory of Microbial Physiological and Metabolic Engineering, State Key Laboratory of Microbial Resources, Institute of Microbiology, Chinese Academy of Sciences, Beijing 100101, China. 2University of Chinese Academy of Sciences, Beijing 100049, China. 3Key Laboratory of Biofuels, Qingdao Institute of Bioenergy and Bioprocess Technology, Chinese Academy of Sciences, Qingdao 266101, China. 4Tianjin Institute of Industrial Biotechnology, Chinese Academy of Sciences, Tianjin 300308, China. 5National Center of Technology Innovation for Synthetic Biology, Tianjin 300308, China. 6Institutional e-mail: ; Center for Shared Technologies and Facilities, Institute of Microbiology, Chinese Academy of Sciences, Beijing 100101, China. ; ; ; Nature Communications | (2022)13:5608 1 Article https://doi.org/10.1038/s41467-022-33358-x Fig. 1 | The structure of marine microbial ecosystems and synthetic microbial communities. a Schematic representation of marine microbial ecosystems structured by primary producers, primary degraders and ultimate consumers. Primary producers in the euphotic zone absorb solar energy and store it in the form of organic matter. Primary degraders in sediments degrade complex organic compounds into small organic compounds. Ultimate consumers in deep sediments oxidize small organic compounds completely through anaerobic respiration with NO3-, Mn4+, Fe3+, SO42- as electron acceptors. During these processes, the electron flow supports microbial growth, metabolism and cycling of elements. b Three synthetic microbial communities, including the two-species (C+S), three-species (C+E+S) and four-species (C+E+S+G) systems, were designed for photoelectric conversion. A sucrose-secreting strain of cyanobacteria was chosen as the primary producer, E. coli was chosen as the primary degrader, while S. oneidensis and G. sulfurreducens were used as the ultimate consumers. Electricity is generated by S. oneidensis and G. sulfurreducens through anaerobic respiration with an electrode as terminal electron acceptor. Among the three synthetic microbial communities, the four-species microbial community is the system completely mimicking the structure of the marine microbial ecosystems and forms the basis of the miniaturized bionic ocean-battery. carbon fixation and remineralization of organic matter, the microbial communities that dominate the marine ecosystems drive biogeochemical cycles and solar energy conversion1,13. From the perspective of energy, marine microbial ecosystems can be viewed as a huge rechargeable battery charged by solar energy, in which the charging and discharging processes are cycled. In the charging process, the photosynthetic microorganisms in the ocean’s surface use solar energy to fix carbon dioxide into organic matter. In the discharging process, the charged energy (in the form of chemical bonds) flows into different microbial species of the ecosystems via step-wise degradation of organic matter by heterotrophic microorganisms, eventually releasing carbon dioxide. These repeated charging/discharging cycles provide energy to all living organisms and sustain their lives in the marine microbial ecosystems. For this huge solar energy conversion system, we coin the term ocean-battery. The majority of heterotrophic microorganisms in the marine microbial ecosystems reside in the upper sediment layers of the seafloor10,12. The average depth of the water column in the ocean is 4000 m, but photosynthesis only occurs in the top 200 m reached by sunlight (Fig. 1a)12. This means that the distance from the primary production to ultimate oxidation exceeds thousands of meters. Due to the large spatial scale of the charging and discharging processes of the ocean-battery, the organic matter deposited from the ocean’s surface is recycled at a geological timescale of (...truncated)