All roads lead to Rome: Cyclic di-GMP differentially regulates extracellular electron transfer in Geobacter biofilms

Yidan Hu; Xi Han; Ying Luo; Jie Jiang; Yongguang Jiang; Bin Cao; Yiran Dong; Liang Shi

doi:10.59717/j.xinn-life.2024.100052

The Innovation Life > 2024 Vol. 2 > No. 1 > 100052

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All roads lead to Rome: Cyclic di-GMP differentially regulates extracellular electron transfer in Geobacter biofilms

1.
Department of Biological Sciences and Technology, School of Environmental Studies, China University of Geosciences, Wuhan 430074, China
2.
Singapore Centre for Environmental Life Sciences Engineering; School of Civil and Environmental Engineering, Nanyang Technological University, 639798, Singapore
3.
State Key Laboratory of Biogeology and Environmental Geology, China University of Geosciences, Wuhan 430074, China
4.
These authors contributed equally

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Corresponding author: liang.shi@cug.edu.cn
Received Date: 19 October 2023

Accepted Date: 03 January 2024

Published Online: 01 February 2024

The Innovation Life 2(1), https://doi.org/10.59717/j.xinn-life.2024.100052 | Cite this article

GRAPHICAL ABSTRACT

GRAPHICAL ABSTRACT

PUBLIC SUMMARY

PUBLIC SUMMARY
1. Microbial extracellular electron transfer is an important biological process.
  
  Geobacter spp. mediates the biogeochemical cycling of elements and shows promise in biotechnology applications.
  
  Cyclic di-GMP, an intracellular secondary messenger, regulates biofilm formation in diverse bacterial species.
  
  Increased or decreased cyclic di-GMP levels both enhance extracellular electron transfer in Geobacter sulfurreducens biofilms.

ABSTRACT

ABSTRACT

Microbial extracellular electron transfer (EET) in dissimilatory metal-reducing microorganisms (DMRMs) is a widespread biological process and is involved in biogeochemical cycling of a variety of elements on the planet of Earth. However, the regulatory networks controlling such important process have been under-investigated. Here, we reported that the intracellular messenger bis-(3′-5′) cyclic dimeric guanosine monophosphate (c-di-GMP) signaling network controls EET in Geobacter sulfurreducens. The low and high levels of c-di-GMP both improved EET in G. sulfurreducens electrode-respiring biofilms by differentially regulating the expression of EET-associated genes. In particular, we found that a low c-di-GMP level reduced the formation of the anode biofilm but enhanced EET by upregulating the transcription of all known nanowire genes (i.e., pilA, omcS, omcZ and omcE). Upregulated omcZ transcription was further determined to play a decisive role in improving EET. Given that c-di-GMP is present in diverse DMRMs, this study substantially expands our understanding of the regulatory role of c-di-GMP signaling and the varied strategies for efficient EET employed by DMRMs. In addition to be fundamentally significant to understand microbe-mineral and microbe-microbe interactions driven by EET, it is also instructive to develop effective engineered microbial systems for practical applications.

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Hu Y., Han X., Luo Y., et al., (2024). All roads lead to Rome: Cyclic di-GMP differentially regulates extracellular electron transfer in Geobacter biofilms. The Innovation Life 2(1): 100052. https://doi.org/10.59717/j.xinn-life.2024.100052

Hu Y., Han X., Luo Y., et al., (2024). All roads lead to Rome: Cyclic di-GMP differentially regulates extracellular electron transfer in Geobacter biofilms. The Innovation Life 2(1): 100052. https://doi.org/10.59717/j.xinn-life.2024.100052

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