Pamela Lyon

Bioelectricity and the Evolution of Multicellular Individuality: Hints from the Microworld

The role of bioelectricity in tissue regeneration in multicellular organisms is now well established and its roles in embryonic development, cancer growth and wound healing are being actively investigated.1-5 Ion channels and bioelectricity mediated by ion channels are found in all known free-living cells, however.6 This is why bacteria and unicellular eukaryotes (e.g., yeast) are being studied as potential generators of usable bioelectricity.7-9 A bacterial ion channel provided the basis for the Nobel Prize-winning elucidation of how neuronal ion channels work.10 A bacterial ion channel— Gloeobacter Ligand-gated Ion Channel (GLIC)—is now the go-to model for investigating the mechanisms of anaesthesia,11-13 long a biomedical mystery and believed to throw light on another famous biological mystery: consciousness (of which we shall not speak). The paper will explore the ancient origins of ion channel-mediated bioelectricity and its possible role in the evolution of multicellular individuality using two principal examples. First is Bacillus subtilis biofilms, communities of thousands of bacterial cells that behave collectively, research into which pioneered the contemporary field of microbial bioelectricity. Next is the ‘slug’ stage of development in the eukaryotic social amoebae Dictyostelium discoideum, in which thousands of formerly free-living cells combine into an individual unit capable of motility. Polymathic developmental biologist Michael Levin has described bioelectricity as the ‘cognitive glue’ enabling cellular collectives to make developmental decisions and behave as a coherent unit at vastly differing scales, from cellular aggregates in prokaryotes and microbial eukaryotes to tissues in multicellular organisms to individual organisms.14 This is an argument in support of that proposition.

Keywords: bioelectricity, ion channels, evolution, Bacillus subtilis, Dictyostelium discoideum, anaesthesia

References

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2 Harris, M. P. Bioelectric signaling as a unique regulator of development and regeneration. Development 148 (2021). https://doi.org/10.1242/dev.180794

3 McMillen, P., Oudin, M. J., Levin, M. & Payne, S. L. Beyond Neurons: Long Distance Communication in Development and Cancer. Frontiers in Cell and Developmental Biology 9 (2021). https://doi.org/10.3389/fcell.2021.739024

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6 Martinac, B., Saimi, Y. & Kung, C. Ion Channels in Microbes. Physiological Reviews 88, 1449-1490 (2008). https://doi.org/10.1152/physrev.00005.2008

7 Bazina, N., Ahmed, T. G., Almdaaf, M., Jibia, S. & Sarker, M. Power generation from wastewater using microbial fuel cells: A review. Journal of Biotechnology 374, 17-30 (2023). https://doi.org/https://doi.org/10.1016/j.jbiotec.2023.07.006

8 Pandit, S. et al. Agricultural Waste and Wastewater as Feedstock for Bioelectricity Generation Using Microbial Fuel Cells: Recent Advances. Fermentation 7, 169 (2021).

9 Enamala, M. K. et al. Photosynthetic microorganisms (Algae) mediated bioelectricity generation in microbial fuel cell: Concise review. Environmental Technology & Innovation 19, 100959 (2020). https://doi.org/https://doi.org/10.1016/j.eti.2020.100959

10 MacKinnon, R. Potassium channels and the atomic basis of selective ion conduction. Nobel Prize Speeches (2003). https://www.nobelprize.org/uploads/2018/06/mackinnon-lecture.pdf.

11 Ouyang, W., Jih, T.-Y., Zhang, T.-T., Correa, A. M. & Hemmings, H. C. Isoflurane Inhibits NaChBac, a Prokaryotic Voltage-Gated Sodium Channel. Journal of Pharmacology and Experimental Therapeutics 322, 1076-1083 (2007). https://doi.org/10.1124/jpet.107.122929

12 Sonner, J. M. A Hypothesis on the Origin and Evolution of the Response to Inhaled Anesthetics. Anesthesia & Analgesia 107, 849-854 (2008). https://doi.org/10.1213/ane.0b013e31817ee684

13 Hemmings, H. C. et al. Towards a Comprehensive Understanding of Anesthetic Mechanisms of Action: A Decade of Discovery. Trends in Pharmacological Sciences 40, 464-481 (2019). https://doi.org/https://doi.org/10.1016/j.tips.2019.05.001

14 Levin, M. Bioelectric networks: the cognitive glue enabling evolutionary scaling from physiology to mind. Animal Cognition 26, 1865-1891 (2023). https://doi.org/10.1007/s10071-023-01780-3