Division of labor and growth during electrical cooperation in multicellular cable bacteria
| Autor: | Michiel V. M. Kienhuis, Diana Vasquez-Cardenas, Cheryl Karman, Silvia Hidalgo-Martinez, Lubos Polerecky, Jack J. Middelburg, Karolien De Wael, Karel S. As, Filip J. R. Meysman, Henricus T. S. Boschker, Stanislav Trashin, Nicole M. J. Geerlings |
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| Přispěvatelé: | Geochemistry, GeoLab Algemeen, Bio-, hydro-, and environmental geochemistry |
| Jazyk: | angličtina |
| Rok vydání: | 2020 |
| Předmět: |
Deltaproteobacteria
Stable isotope probing Spectrometry Mass Secondary Ion Sulfides Microbiology Redox Electron Transport 03 medical and health sciences Electron transfer Electricity Ammonia Cable bacteria NanoSIMS stable isotope probing Biology nanoSIMS 030304 developmental biology Carbon Isotopes 0303 health sciences Multidisciplinary biology 030306 microbiology Chemistry Assimilation (biology) Metabolism Biological Sciences multicellularity biology.organism_classification Anoxic waters Electron transport chain Multicellular organism cable bacteria Biophysics Multicellularity metabolism Engineering sciences. Technology Bacteria |
| Zdroj: | Proceedings of the National Academy of Sciences of the United States of America PNAS, 17(10), 5478. National Academy of Sciences Proceedings of the National Academy of Sciences of the United States of America, 117(10) |
| ISSN: | 0027-8424 |
| Popis: | Significance Cable bacteria form centimeter-long, multicellular filaments whose energy metabolism involves cooperation among cells that separately perform oxidation of the electron donor and reduction of the electron acceptor. This cooperative division of labor is facilitated via long-range electrical currents that run from cell to cell along a network of conductive fibers. Here we show that biomass synthesis shows a surprising asymmetry along the filament: only the cells oxidizing the electron donor conserve energy for growth, while the other cells reduce electron acceptors without biosynthesis. Our study hence provides insights into the physiology of an unconventional chemolithotroph, which forms a multicellular electrically connected system with unique functional differentiation, integration, and coordination. Multicellularity is a key evolutionary innovation, leading to coordinated activity and resource sharing among cells, which generally occurs via the physical exchange of chemical compounds. However, filamentous cable bacteria display a unique metabolism in which redox transformations in distant cells are coupled via long-distance electron transport rather than an exchange of chemicals. This challenges our understanding of organismal functioning, as the link among electron transfer, metabolism, energy conservation, and filament growth in cable bacteria remains enigmatic. Here, we show that cells within individual filaments of cable bacteria display a remarkable dichotomy in biosynthesis that coincides with redox zonation. Nanoscale secondary ion mass spectrometry combined with 13C (bicarbonate and propionate) and 15N-ammonia isotope labeling reveals that cells performing sulfide oxidation in deeper anoxic horizons have a high assimilation rate, whereas cells performing oxygen reduction in the oxic zone show very little or no label uptake. Accordingly, oxygen reduction appears to merely function as a mechanism to quickly dispense of electrons with little to no energy conservation, while biosynthesis and growth are restricted to sulfide-respiring cells. Still, cells can immediately switch roles when redox conditions change, and show no differentiation, which suggests that the “community service” performed by the cells in the oxic zone is only temporary. Overall, our data reveal a division of labor and electrical cooperation among cells that has not been seen previously in multicellular organisms. |
| Databáze: | OpenAIRE |
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