Records |
Author |
Geerlings, N.M.J.; Karman, C.; Trashin, S.; As, K.S.; Kienhuis, M.V.M.; Hidalgo-Martinez, S.; Vasquez-Cardenas, D.; Boschker, H.T.S.; De Wael, K.; Middelburg, J.J.; Polerecky, L.; Meysman, F.J.R. |
Title |
Division of labor and growth during electrical cooperation in multicellular cable bacteria |
Type |
A1 Journal article |
Year |
2020 |
Publication |
Proceedings Of The National Academy Of Sciences Of The United States Of America |
Abbreviated Journal |
P Natl Acad Sci Usa |
Volume |
117 |
Issue |
10 |
Pages |
5478-5485 |
Keywords |
A1 Journal article; Engineering sciences. Technology; AXES (Antwerp X-ray Analysis, Electrochemistry and Speciation) |
Abstract |
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 13 C (bicarbonate and propionate) and 15 N-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. |
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Corporate Author |
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Thesis |
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Publisher |
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Place of Publication |
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Editor |
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Language |
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Wos |
000519530400054 |
Publication Date |
2020-02-25 |
Series Editor |
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Series Title |
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Abbreviated Series Title |
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Series Volume |
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Series Issue |
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Edition |
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ISSN |
0027-8424; 1091-6490 |
ISBN |
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Additional Links |
UA library record; WoS full record; WoS citing articles |
Impact Factor |
11.1 |
Times cited |
6 |
Open Access |
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Notes ![sorted by Notes field, descending order (down)](img/sort_desc.gif) |
; We thank Arnold van Dijk for helping with the GasBench isotope ratio mass spectrometry analysis. N.M.J.G. is the recipient of a Ph.D. scholarship for teachers from the Netherlands Organisation for Scientific Research (NWO) in the Netherlands (grant 023.005.049). K.S.A. received financial support from the Olaf Schuiling fund. F.J.R.M. was financially supported by the Research Foundation Flanders (FWO) via grant G043119N, and the Netherlands Organization for Scientific Research (VICI grant 016.VICI.170.072). J.J.M. was supported by the Ministry of Education via the Netherlands Earth System Science Centre. The NanoSIMS facility was partly supported by an NWO large infrastructure subsidy to J.J.M. (175.010.2009.011). ; |
Approved |
Most recent IF: 11.1; 2020 IF: 9.661 |
Call Number |
UA @ admin @ c:irua:166452 |
Serial |
6487 |
Permanent link to this record |
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Author |
Meysman, F.J.R.; Cornelissen, R.; Trashin, S.; Bonne, R.; Hidalgo-Martinez, S.; van der Veen, J.; Blom, C.J.; Karman, C.; Hou, J.-L.; Eachambadi, R.T.; Geelhoed, J.S.; De Wael, K.; Beaumont, H.J.E.; Cleuren, B.; Valcke, R.; van der Zant, H.S.J.; Boschker, H.T.S.; Manca, J.V. |
Title |
A highly conductive fibre network enables centimetre-scale electron transport in multicellular cable bacteria |
Type |
A1 Journal article |
Year |
2019 |
Publication |
Nature communications |
Abbreviated Journal |
Nat Commun |
Volume |
10 |
Issue |
10 |
Pages |
4120 |
Keywords |
A1 Journal article; Engineering sciences. Technology; AXES (Antwerp X-ray Analysis, Electrochemistry and Speciation) |
Abstract |
Biological electron transport is classically thought to occur over nanometre distances, yet recent studies suggest that electrical currents can run along centimetre-long cable bacteria. The phenomenon remains elusive, however, as currents have not been directly measured, nor have the conductive structures been identified. Here we demonstrate that cable bacteria conduct electrons over centimetre distances via highly conductive fibres embedded in the cell envelope. Direct electrode measurements reveal nanoampere currents in intact filaments up to 10.1 mm long (>2000 adjacent cells). A network of parallel periplasmic fibres displays a high conductivity (up to 79 S cm(-1)), explaining currents measured through intact filaments. Conductance rapidly declines upon exposure to air, but remains stable under vacuum, demonstrating that charge transfer is electronic rather than ionic. Our finding of a biological structure that efficiently guides electrical currents over long distances greatly expands the paradigm of biological charge transport and could enable new bio-electronic applications. |
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Corporate Author |
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Thesis |
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Publisher |
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Place of Publication |
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Language |
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Wos |
000485216900006 |
Publication Date |
2019-09-11 |
Series Editor |
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Series Title |
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Abbreviated Series Title |
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Series Volume |
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Series Issue |
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Edition |
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ISSN |
2041-1723 |
ISBN |
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Additional Links |
UA library record; WoS full record; WoS citing articles |
Impact Factor |
12.124 |
Times cited |
10 |
Open Access |
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Notes ![sorted by Notes field, descending order (down)](img/sort_desc.gif) |
; This research was financially supported by the European Research Council under the European Union's Seventh Framework Programme (FP/2007-2013) through ERC Grant 306933 (F.J.R.M.), the Research Foundation Flanders (FWO project grant G031416N), and the Netherlands Organisation for Scientific Research (VICI grant 016.VICI.170.072 to F.J.R.M.). H.J.E.B., C.J.B. and H.S.J.Z. were supported by the Netherlands Organisation for Scientific Research (NWO/OCW), as part of the Frontiers of Nanoscience program. R.B. is supported by an 'aspirant' grant from Research Foundation Flanders (FWO). We thank Laurine Burdorf (UAntwerpen) for help with Thiothrix cultivation, Marlies Nijemeisland (Faculty of Aerospace, TU Delft) for assistance with Raman microscopy, and Jan D'Haen (UHasselt) and Renaat Dasseville (UGent) for help with EM imaging. ; |
Approved |
Most recent IF: 12.124 |
Call Number |
UA @ admin @ c:irua:162795 |
Serial |
5451 |
Permanent link to this record |
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Author |
Pankratov, D.; Hidalgo Martinez, S.; Karman, C.; Gerzhik, A.; Gomila, G.; Trashin, S.; Boschker, H.T.S.; Geelhoed, J.S.; Mayer, D.; De Wael, K.; Meysman, F.J.R. |
Title |
The organo-metal-like nature of long-range conduction in cable bacteria |
Type |
A1 Journal article |
Year |
2024 |
Publication |
Bioelectrochemistry: an international journal devoted to electrochemical aspects of biology and biological aspects of electrochemistry |
Abbreviated Journal |
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Volume |
157 |
Issue |
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Pages |
108675-10 |
Keywords |
A1 Journal article |
Abstract |
Cable bacteria are filamentous, multicellular microorganisms that display an exceptional form of biological electron transport across centimeter-scale distances. Currents are guided through a network of nickel-containing protein fibers within the cell envelope. Still, the mechanism of long-range conduction remains unresolved. Here, we characterize the conductance of the fiber network under dry and wet, physiologically relevant, conditions. Our data reveal that the fiber conductivity is high (median value: 27 S cm−1; range: 2 to 564 S cm−1), does not show any redox signature, has a low thermal activation energy (Ea = 69 ± 23 meV), and is not affected by humidity or the presence of ions. These features set the nickel-based conduction mechanism in cable bacteria apart from other known forms of biological electron transport. As such, conduction resembles that of an organic semi-metal with a high charge carrier density. Our observation that biochemistry can synthesize an organo-metal-like structure opens the way for novel bio-based electronic technologies. |
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Place of Publication |
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Wos |
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Publication Date |
2024-02-25 |
Series Editor |
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Series Title |
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Abbreviated Series Title |
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Series Volume |
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Series Issue |
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Edition |
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ISSN |
1567-5394 |
ISBN |
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Additional Links |
UA library record |
Impact Factor |
5 |
Times cited |
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Open Access |
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Notes ![sorted by Notes field, descending order (down)](img/sort_desc.gif) |
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Approved |
Most recent IF: 5; 2024 IF: 3.346 |
Call Number |
UA @ admin @ c:irua:205117 |
Serial |
9215 |
Permanent link to this record |