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5. Multi-wavelength Raman microscopy of nickel-based electron transport in cable bacteria

Author

Smets, Bent, Boschker, Henricus T.S., Wetherington, Maxwell T., Lelong, Gérald, Hidalgo-Martinez, Silvia, Polerecky, Lubos, Nuyts, Gert, De wael, Karolien, Meysman, Filip J.R., Smets, Bent, Boschker, Henricus T.S., Wetherington, Maxwell T., Lelong, Gérald, Hidalgo-Martinez, Silvia, Polerecky, Lubos, Nuyts, Gert, De wael, Karolien, and Meysman, Filip J.R.

Abstract

Cable bacteria embed a network of conductive protein fibers in their cell envelope that efficiently guides electron transport over distances spanning up to several centimeters. This form of long-distance electron transport is unique in biology and is mediated by a metalloprotein with a sulfur-coordinated nickel (Ni) cofactor. However, the molecular structure of this cofactor remains presently unknown. Here, we applied multi-wavelength Raman microscopy to identify cell compounds linked to the unique cable bacterium physiology, combined with stable isotope labeling, and orientation-dependent and ultralow-frequency Raman microscopy to gain insight into the structure and organization of this novel Ni-cofactor. Raman spectra of native cable bacterium filaments reveal vibrational modes originating from cytochromes, polyphosphate granules, proteins, as well as the Ni-cofactor. After selective extraction of the conductive fiber network from the cell envelope, the Raman spectrum becomes simpler, and primarily retains vibrational modes associated with the Ni-cofactor. These Ni-cofactor modes exhibit intense Raman scattering as well as a strong orientation-dependent response. The signal intensity is particularly elevated when the polarization of incident laser light is parallel to the direction of the conductive fibers. This orientation dependence allows to selectively identify the modes that are associated with the Ni-cofactor. We identified 13 such modes, some of which display strong Raman signals across the entire range of applied wavelengths (405–1,064 nm). Assignment of vibrational modes, supported by stable isotope labeling, suggest that the structure of the Ni-cofactor shares a resemblance with that of nickel bis(1,2-dithiolene) complexes. Overall, our results indicate that cable bacteria have evolved a unique cofactor structure that does not resemble any of the known Ni-cofactors in biology.

Published
2024

6. Multi-wavelength Raman microscopy of nickel-based electron transport in cable bacteria

Author

IVAU: Instituut voor Aardwetenschappen Utrecht, Geochemistry, Smets, Bent, Boschker, Henricus T.S., Wetherington, Maxwell T., Lelong, Gérald, Hidalgo-Martinez, Silvia, Polerecky, Lubos, Nuyts, Gert, De wael, Karolien, Meysman, Filip J.R., IVAU: Instituut voor Aardwetenschappen Utrecht, Geochemistry, Smets, Bent, Boschker, Henricus T.S., Wetherington, Maxwell T., Lelong, Gérald, Hidalgo-Martinez, Silvia, Polerecky, Lubos, Nuyts, Gert, De wael, Karolien, and Meysman, Filip J.R.

Published
2024

14. Cable Bacteria Get Energy Through Electrical Teamwork

Author

Geerlings, Nicole M.J., Middelburg, Jack J., Polerecky, Lubos, Meysman, Filip J.R., Geerlings, Nicole M.J., Middelburg, Jack J., Polerecky, Lubos, and Meysman, Filip J.R.

Abstract

Cable bacteria are very different from most other bacteria. First of all, they are multicellular, and each cable bacterium has tens of thousands of cells connected in a chain called a filament that can be several centimeters long. What makes cable bacteria really special is the way they get the energy they need for living: the cells within a filament have to work together to generate energy, and this involves electricity! In this article, we will describe these fascinating bacteria and tell you about recent research that shows how the cells within a filament work together.

Published
2023

15. Cable Bacteria Get Energy Through Electrical Teamwork

Author

Bio-, hydro-, and environmental geochemistry, Geochemistry, Geerlings, Nicole M.J., Middelburg, Jack J., Polerecky, Lubos, Meysman, Filip J.R., Bio-, hydro-, and environmental geochemistry, Geochemistry, Geerlings, Nicole M.J., Middelburg, Jack J., Polerecky, Lubos, and Meysman, Filip J.R.

Published
2023

19. Global maps of soil temperature

Author

Lembrechts, Jonas J., van den Hoogen, Johan, Aalto, Juha, Ashcroft, Michael B., De Frenne, Pieter, Kemppinen, Julia, Kopecký, Martin, Luoto, Miska, Maclean, Ilya M. D., Crowther, Thomas W., Bailey, Joseph J., Haesen, Stef, Klinges, David H., Niittynen, Pekka, Scheffers, Brett R., Van Meerbeek, Koenraad, Aartsma, Peter, Abdalaze, Otar, Abedi, Mehdi, Aerts, Rien, Ahmadian, Negar, Ahrends, Antje, Alatalo, Juha M., Alexander, Jake M., Allonsius, Camille Nina, Altman, Jan, Ammann, Christof, Andres, Christian, Andrews, Christopher, Ardö, Jonas, Arriga, Nicola, Arzac, Alberto, Aschero, Valeria, Assis, Rafael L., Assmann, Jakob Johann, Bader, Maaike Y., Bahalkeh, Khadijeh, Barančok, Peter, Barrio, Isabel C., Barros, Agustina, Barthel, Matti, Basham, Edmund W., Bauters, Marijn, Bazzichetto, Manuele, Belelli Marchesini, Luca, Bell, Michael C., Benavides, Juan C., Benito Alonso, José Luis, Berauer, Bernd J., Bjerke, Jarle W., Björk, Robert G., Björkman, Mats P., Björnsdóttir, Katrin, Blonder, Benjamin, Boeckx, Pascal, Boike, Julia, Bokhorst, Stef, Brum, Bárbara N. S., Brůna, Josef, Buchmann, Nina, Buysse, Pauline, Camargo, Jose Luis C., Campoe, Otavio, Candan, Onur, Canessa, Rafaella, Cannone, Nicoletta, Carbognani, Michele, Carnicer, Jofre, Casanova-Katny, Angélica, Cesarz, Simone, Chojnicki, Bogdan, Choler, Philippe, Chown, Steven L., Cifuentes, Edgar F., Čiliak, Marek, Contador, Tamara, Convey, Peter, Cooper, Elisabeth J., Cremonese, Eodardo, Curasi, Salvatore R., Curtis, Robin, Cutini, Maurizio, Dahlberg, C. Johan, Daskalova, Gergana N., de Pablo, Miguel Angel, Della Chiesa, Stefano, Dengler, Jürgen, Deronde, Bart, Di Cecco, Valter, Di Musciano, Michele, Dick, Jan, Dimarco, Romina D., Dolezal, Jiri, Dorrepaal, Ellen, Dusek, Jiri, Eisenhauer, Nico, Eklundh, Lars, Erickson, Todd E., Erschbamer, Brigitta, Eugster, Werner, Ewers, Robert M., Exton, Dan A., Fanin, Nicolas, Fazlioglu, Fatih, Feigenwinter, Iris, Fenu, Giuseppe, Ferlian, Olga, Fernández Calzado, M. Rosa, Fernández-Pascual, Eduardo, Finckh, Manfred, Finger Higgens, Rebecca, Forte, T'ai G. W., Freeman, Erika C., Frei, Esther R., Fuentes-Lillo, Eduardo, García, Rafael A., García, María B., Géron, Charly, Gharun, Mana, Ghosn, Dany, Gigauri, Khatuna, Gobin, Anne, Goded, Ignacio, Goeckede, Mathias, Gottschall, Felix, Goulding, Keith, Govaert, Sanne, Jessen Graae, Bente, Greenwood, Sarah, Greiser, Caroline, Grelle, Achim, Guénard, Benoït, Guglielmin, Mauro, Guillemot, Joannès, Haase, Peter, Haider, Sylvia, Halbritter, Aud H., Hamid, Maroof, Hammerle, Albin, Hampe, Arndt, Haugum, Siri V., Hederová, Lucia, Heinesch, Bernard, Helfters, Carole, Hepenstrick, Daniel, Herberich, Maximiliane, Herbst, Mathias, Hermanutz, Luise, Hik, David S., Hoffrén, Raúl, Homeier, Jürgen, Hörtnagl, Lukas, Hoye, Toke T., Hrbacek, Filip, Hylander, Kristoffer, Iwata, Hiroki, Jackowicz-Korczynski, Marcin, Jactel, Hervé, Järveoja, Järvi, Jastrzębowski, Szymon, Jentsch, Anke, Jiménez, Juan J., Jónsdóttir, Ingibjörg S., Jucker, Tommaso, Jump, Alistair S., Juszczak, Radoslaw, Kanka, Robert, Kašpar, Vít, Kazakis, George, Kelly, Julia, Khuroo, Anzar A., Klemedtsson, Leif, Klisz, Marcin, Kljun, Natascha, Knohl, Alexander, Kobler, Johannes, Kollár, Jozef, Kotowska, Martyna M., Kovács, Bence, Kreyling, Juergen, Lamprecht, Andrea, Lang, Simone I., Larson, Christian, Larson, Keith, Laska, Kamil, Le Maire, Guerric, Leihy, Rachel I., Lens, Luc, Liljebladh, Bengt, Lohila, Annalea, Lorite, Juan, Loubet, Benjamin, Lynn, Joshua, Macek, Martin, Mackenzie, Roy, Magliulo, Enzo, Maier, Regine, Malfasi, Francesco, Malis, František, Man, Matěj, Manca, Giovanni, Manco, Antonio, Manise, Tanguy, Manolaki, Paraskevi, Marciniak, Felipe, Matula, Radim, Mazzolari, Ana Clara, Medinets, Volodymyr, Meeussen, Camille, Merinero, Sonia, de Cássia Guimarães Mesquita, Rita, Meusburger, Katrin, Meysman, Filip J.R., Michaletz, Sean T., Milbau, Ann, Moiseev, Dmitry, Moiseev, Pavel, Mondoni, Andrea, Monfries, Ruth, Montagnani, Leonardo, Moriana-Armendariz, Mikel, Morra di Cella, Umberto, Mörsdorf, Martin, Mosedale, Jonnathan R., Muffler, Lena, Muñoz-Rojas, Miriam, Myers, Jonnathan A., Myers-Smith, Isla H., Nagy, Laszlo, Nardino, Marianna, Naujokaitis-Lewis, Ilona, Newling, Emily, Nicklas, Lena, Niedrist, Georg, Niessner, Armin, Nilsson, Mats B., Normand, Signe, Nosetto, Marcelo, Nouvellon, Yann, Nunez, Martin, Ogaya, Romà, Ogée, Jérôme, Okello, Joseph, Olejnik, Janusz, Olesen, Jørgen Eivind, Opedal, Oystein H., Orsenigo, Simone, Palaj, Andrej, Pampuch, Timo, Panov, Alexey V., Pärtel, Meelis, Pastor, Ada, Pauchard, Anibal, Pauli, Harald, Pavelka, Marian, Pearse, William D., Peichl, Matthias, Pellissier, Loïc, Penczykowski, Rachel M., Peñuelas, Josep, Petit Bon, Matteo, Petraglia, Alessandro, Phartyal, Shyam S., Phoenix, Gareth K., Pio, Casimiro, Pitacco, Andrea, Pitteloud, Camille, Plichta, Roman, Porro, Francesco, Portillo-Estrada, Miguel, Poulenard, Jérôme, Poyatos, Rafael, Prokushkin, Anatoly S., Puchalka, Radoslaw, Puscas, Mihai, Radujković, Dajana, Randall, Krystal, Ratier Backes, Amanda, Remmele, Sabine, Remmers, Wolfram, Renault, David, Risch, Anita C., Rixen, Christian, Robinson, Sharon A., Robroek, Bjorn J.M., Rocha, Adrian V., Rossi, Christian, Rossi, Graziano, Roupsard, Olivier, et al., Lembrechts, Jonas J., van den Hoogen, Johan, Aalto, Juha, Ashcroft, Michael B., De Frenne, Pieter, Kemppinen, Julia, Kopecký, Martin, Luoto, Miska, Maclean, Ilya M. D., Crowther, Thomas W., Bailey, Joseph J., Haesen, Stef, Klinges, David H., Niittynen, Pekka, Scheffers, Brett R., Van Meerbeek, Koenraad, Aartsma, Peter, Abdalaze, Otar, Abedi, Mehdi, Aerts, Rien, Ahmadian, Negar, Ahrends, Antje, Alatalo, Juha M., Alexander, Jake M., Allonsius, Camille Nina, Altman, Jan, Ammann, Christof, Andres, Christian, Andrews, Christopher, Ardö, Jonas, Arriga, Nicola, Arzac, Alberto, Aschero, Valeria, Assis, Rafael L., Assmann, Jakob Johann, Bader, Maaike Y., Bahalkeh, Khadijeh, Barančok, Peter, Barrio, Isabel C., Barros, Agustina, Barthel, Matti, Basham, Edmund W., Bauters, Marijn, Bazzichetto, Manuele, Belelli Marchesini, Luca, Bell, Michael C., Benavides, Juan C., Benito Alonso, José Luis, Berauer, Bernd J., Bjerke, Jarle W., Björk, Robert G., Björkman, Mats P., Björnsdóttir, Katrin, Blonder, Benjamin, Boeckx, Pascal, Boike, Julia, Bokhorst, Stef, Brum, Bárbara N. S., Brůna, Josef, Buchmann, Nina, Buysse, Pauline, Camargo, Jose Luis C., Campoe, Otavio, Candan, Onur, Canessa, Rafaella, Cannone, Nicoletta, Carbognani, Michele, Carnicer, Jofre, Casanova-Katny, Angélica, Cesarz, Simone, Chojnicki, Bogdan, Choler, Philippe, Chown, Steven L., Cifuentes, Edgar F., Čiliak, Marek, Contador, Tamara, Convey, Peter, Cooper, Elisabeth J., Cremonese, Eodardo, Curasi, Salvatore R., Curtis, Robin, Cutini, Maurizio, Dahlberg, C. Johan, Daskalova, Gergana N., de Pablo, Miguel Angel, Della Chiesa, Stefano, Dengler, Jürgen, Deronde, Bart, Di Cecco, Valter, Di Musciano, Michele, Dick, Jan, Dimarco, Romina D., Dolezal, Jiri, Dorrepaal, Ellen, Dusek, Jiri, Eisenhauer, Nico, Eklundh, Lars, Erickson, Todd E., Erschbamer, Brigitta, Eugster, Werner, Ewers, Robert M., Exton, Dan A., Fanin, Nicolas, Fazlioglu, Fatih, Feigenwinter, Iris, Fenu, Giuseppe, Ferlian, Olga, Fernández Calzado, M. Rosa, Fernández-Pascual, Eduardo, Finckh, Manfred, Finger Higgens, Rebecca, Forte, T'ai G. W., Freeman, Erika C., Frei, Esther R., Fuentes-Lillo, Eduardo, García, Rafael A., García, María B., Géron, Charly, Gharun, Mana, Ghosn, Dany, Gigauri, Khatuna, Gobin, Anne, Goded, Ignacio, Goeckede, Mathias, Gottschall, Felix, Goulding, Keith, Govaert, Sanne, Jessen Graae, Bente, Greenwood, Sarah, Greiser, Caroline, Grelle, Achim, Guénard, Benoït, Guglielmin, Mauro, Guillemot, Joannès, Haase, Peter, Haider, Sylvia, Halbritter, Aud H., Hamid, Maroof, Hammerle, Albin, Hampe, Arndt, Haugum, Siri V., Hederová, Lucia, Heinesch, Bernard, Helfters, Carole, Hepenstrick, Daniel, Herberich, Maximiliane, Herbst, Mathias, Hermanutz, Luise, Hik, David S., Hoffrén, Raúl, Homeier, Jürgen, Hörtnagl, Lukas, Hoye, Toke T., Hrbacek, Filip, Hylander, Kristoffer, Iwata, Hiroki, Jackowicz-Korczynski, Marcin, Jactel, Hervé, Järveoja, Järvi, Jastrzębowski, Szymon, Jentsch, Anke, Jiménez, Juan J., Jónsdóttir, Ingibjörg S., Jucker, Tommaso, Jump, Alistair S., Juszczak, Radoslaw, Kanka, Robert, Kašpar, Vít, Kazakis, George, Kelly, Julia, Khuroo, Anzar A., Klemedtsson, Leif, Klisz, Marcin, Kljun, Natascha, Knohl, Alexander, Kobler, Johannes, Kollár, Jozef, Kotowska, Martyna M., Kovács, Bence, Kreyling, Juergen, Lamprecht, Andrea, Lang, Simone I., Larson, Christian, Larson, Keith, Laska, Kamil, Le Maire, Guerric, Leihy, Rachel I., Lens, Luc, Liljebladh, Bengt, Lohila, Annalea, Lorite, Juan, Loubet, Benjamin, Lynn, Joshua, Macek, Martin, Mackenzie, Roy, Magliulo, Enzo, Maier, Regine, Malfasi, Francesco, Malis, František, Man, Matěj, Manca, Giovanni, Manco, Antonio, Manise, Tanguy, Manolaki, Paraskevi, Marciniak, Felipe, Matula, Radim, Mazzolari, Ana Clara, Medinets, Volodymyr, Meeussen, Camille, Merinero, Sonia, de Cássia Guimarães Mesquita, Rita, Meusburger, Katrin, Meysman, Filip J.R., Michaletz, Sean T., Milbau, Ann, Moiseev, Dmitry, Moiseev, Pavel, Mondoni, Andrea, Monfries, Ruth, Montagnani, Leonardo, Moriana-Armendariz, Mikel, Morra di Cella, Umberto, Mörsdorf, Martin, Mosedale, Jonnathan R., Muffler, Lena, Muñoz-Rojas, Miriam, Myers, Jonnathan A., Myers-Smith, Isla H., Nagy, Laszlo, Nardino, Marianna, Naujokaitis-Lewis, Ilona, Newling, Emily, Nicklas, Lena, Niedrist, Georg, Niessner, Armin, Nilsson, Mats B., Normand, Signe, Nosetto, Marcelo, Nouvellon, Yann, Nunez, Martin, Ogaya, Romà, Ogée, Jérôme, Okello, Joseph, Olejnik, Janusz, Olesen, Jørgen Eivind, Opedal, Oystein H., Orsenigo, Simone, Palaj, Andrej, Pampuch, Timo, Panov, Alexey V., Pärtel, Meelis, Pastor, Ada, Pauchard, Anibal, Pauli, Harald, Pavelka, Marian, Pearse, William D., Peichl, Matthias, Pellissier, Loïc, Penczykowski, Rachel M., Peñuelas, Josep, Petit Bon, Matteo, Petraglia, Alessandro, Phartyal, Shyam S., Phoenix, Gareth K., Pio, Casimiro, Pitacco, Andrea, Pitteloud, Camille, Plichta, Roman, Porro, Francesco, Portillo-Estrada, Miguel, Poulenard, Jérôme, Poyatos, Rafael, Prokushkin, Anatoly S., Puchalka, Radoslaw, Puscas, Mihai, Radujković, Dajana, Randall, Krystal, Ratier Backes, Amanda, Remmele, Sabine, Remmers, Wolfram, Renault, David, Risch, Anita C., Rixen, Christian, Robinson, Sharon A., Robroek, Bjorn J.M., Rocha, Adrian V., Rossi, Christian, Rossi, Graziano, Roupsard, Olivier, and et al.

Abstract

Research in global change ecology relies heavily on global climatic grids derived from estimates of air temperature in open areas at around 2 m above the ground. These climatic grids do not reflect conditions below vegetation canopies and near the ground surface, where critical ecosystem functions occur and most terrestrial species reside. Here, we provide global maps of soil temperature and bioclimatic variables at a 1-km2 resolution for 0–5 and 5–15 cm soil depth. These maps were created by calculating the difference (i.e. offset) between in situ soil temperature measurements, based on time series from over 1200 1-km2 pixels (summarized from 8519 unique temperature sensors) across all the world's major terrestrial biomes, and coarse-grained air temperature estimates from ERA5-Land (an atmospheric reanalysis by the European Centre for Medium-Range Weather Forecasts). We show that mean annual soil temperature differs markedly from the corresponding gridded air temperature, by up to 10°C (mean = 3.0 ± 2.1°C), with substantial variation across biomes and seasons. Over the year, soils in cold and/or dry biomes are substantially warmer (+3.6 ± 2.3°C) than gridded air temperature, whereas soils in warm and humid environments are on average slightly cooler (−0.7 ± 2.3°C). The observed substantial and biome-specific offsets emphasize that the projected impacts of climate and climate change on near-surface biodiversity and ecosystem functioning are inaccurately assessed when air rather than soil temperature is used, especially in cold environments. The global soil-related bioclimatic variables provided here are an important step forward for any application in ecology and related disciplines. Nevertheless, we highlight the need to fill remaining geographic gaps by collecting more in situ measurements of microclimate conditions to further enhance the spatiotemporal resolution of global soil temperature products for ecological applications.

Published
2022

21. Cell Cycle, Filament Growth and Synchronized Cell Division in Multicellular Cable Bacteria

Author

Geerlings, Nicole M.J., Geelhoed, Jeanine S., Vasquez-Cardenas, Diana, Kienhuis, Michiel V.M., Hidalgo-Martinez, Silvia, Boschker, Henricus T.S., Middelburg, Jack J., Meysman, Filip J.R., Polerecky, Lubos, Geochemistry, GeoLab Algemeen, Bio-, hydro-, and environmental geochemistry, Geochemistry, GeoLab Algemeen, and Bio-, hydro-, and environmental geochemistry

Subjects
cell division, Microbiology (medical), Cell division, lcsh:QR1-502, Microbiology, lcsh:Microbiology, Protein filament, 03 medical and health sciences, filament growth, Biology, stable isotope probing, 030304 developmental biology, Original Research, nanoSIMS, 0303 health sciences, 030306 microbiology, Chemistry, Cell growth, Cell cycle, Division (mathematics), Electron transport chain, Multicellular organism, cable bacteria, Biophysics, cell cycle, Cell envelope
Abstract

Cable bacteria are multicellular, Gram-negative filamentous bacteria that display a unique division of metabolic labor between cells. Cells in deeper sediment layers are oxidizing sulfide, while cells in the surface layers of the sediment are reducing oxygen. The electrical coupling of these two redox half reactions is ensured via long-distance electron transport through a network of conductive fibers that run in the shared cell envelope of the centimeter-long filament. Here we investigate how this unique electrogenic metabolism is linked to filament growth and cell division. Combining dual-label stable isotope probing (13C and 15N), nanoscale secondary ion mass spectrometry, fluorescence microscopy and genome analysis, we find that the cell cycle of cable bacteria cells is highly comparable to that of other, single-celled Gram-negative bacteria. However, the timing of cell growth and division appears to be tightly and uniquely controlled by long-distance electron transport, as cell division within an individual filament shows a remarkable synchronicity that extends over a millimeter length scale. To explain this, we propose the “oxygen pacemaker” model in which a filament only grows when performing long-distance transport, and the latter is only possible when a filament has access to oxygen so it can discharge electrons from its internal electrical network.

Published
2021

22. Efficient long-range conduction in cable bacteria through nickel protein wires

Author

Boschker, Henricus T.S., Cook, Perran L.M., Polerecky, Lubos, Eachambadi, Raghavendran Thiruvallur, Lozano, Helena, Hidalgo-Martinez, Silvia, Khalenkow, Dmitry, Spampinato, Valentina, Claes, Nathalie, Kundu, Paromita, Wang, Da, Bals, Sara, Sand, Karina K., Cavezza, Francesca, Hauffman, Tom, Bjerg, Jesper Tataru, Skirtach, Andre G., Kochan, Kamila, McKee, Merrilyn, Wood, Bayden, Bedolla, Diana, Gianoncelli, Alessandra, Geerlings, Nicole M.J., Van Gerven, Nani, Remaut, Han, Geelhoed, Jeanine S., Millan-Solsona, Ruben, Fumagalli, Laura, Nielsen, Lars Peter, Franquet, Alexis, Manca, Jean V., Gomila, Gabriel, Meysman, Filip J.R., Boschker, Henricus T.S., Cook, Perran L.M., Polerecky, Lubos, Eachambadi, Raghavendran Thiruvallur, Lozano, Helena, Hidalgo-Martinez, Silvia, Khalenkow, Dmitry, Spampinato, Valentina, Claes, Nathalie, Kundu, Paromita, Wang, Da, Bals, Sara, Sand, Karina K., Cavezza, Francesca, Hauffman, Tom, Bjerg, Jesper Tataru, Skirtach, Andre G., Kochan, Kamila, McKee, Merrilyn, Wood, Bayden, Bedolla, Diana, Gianoncelli, Alessandra, Geerlings, Nicole M.J., Van Gerven, Nani, Remaut, Han, Geelhoed, Jeanine S., Millan-Solsona, Ruben, Fumagalli, Laura, Nielsen, Lars Peter, Franquet, Alexis, Manca, Jean V., Gomila, Gabriel, and Meysman, Filip J.R.

Abstract

Filamentous cable bacteria display long-range electron transport, generating electrical currents over centimeter distances through a highly ordered network of fibers embedded in their cell envelope. The conductivity of these periplasmic wires is exceptionally high for a biological material, but their chemical structure and underlying electron transport mechanism remain unresolved. Here, we combine high-resolution microscopy, spectroscopy, and chemical imaging on individual cable bacterium filaments to demonstrate that the periplasmic wires consist of a conductive protein core surrounded by an insulating protein shell layer. The core proteins contain a sulfur-ligated nickel cofactor, and conductivity decreases when nickel is oxidized or selectively removed. The involvement of nickel as the active metal in biological conduction is remarkable, and suggests a hitherto unknown form of electron transport that enables efficient conduction in centimeter-long protein structures.

Published
2021

23. Efficient long-range conduction in cable bacteria through nickel protein wires

Author

Geochemistry, Bio-, hydro-, and environmental geochemistry, Boschker, Henricus T.S., Cook, Perran L.M., Polerecky, Lubos, Eachambadi, Raghavendran Thiruvallur, Lozano, Helena, Hidalgo-Martinez, Silvia, Khalenkow, Dmitry, Spampinato, Valentina, Claes, Nathalie, Kundu, Paromita, Wang, Da, Bals, Sara, Sand, Karina K., Cavezza, Francesca, Hauffman, Tom, Bjerg, Jesper Tataru, Skirtach, Andre G., Kochan, Kamila, McKee, Merrilyn, Wood, Bayden, Bedolla, Diana, Gianoncelli, Alessandra, Geerlings, Nicole M.J., Van Gerven, Nani, Remaut, Han, Geelhoed, Jeanine S., Millan-Solsona, Ruben, Fumagalli, Laura, Nielsen, Lars Peter, Franquet, Alexis, Manca, Jean V., Gomila, Gabriel, Meysman, Filip J.R., Geochemistry, Bio-, hydro-, and environmental geochemistry, Boschker, Henricus T.S., Cook, Perran L.M., Polerecky, Lubos, Eachambadi, Raghavendran Thiruvallur, Lozano, Helena, Hidalgo-Martinez, Silvia, Khalenkow, Dmitry, Spampinato, Valentina, Claes, Nathalie, Kundu, Paromita, Wang, Da, Bals, Sara, Sand, Karina K., Cavezza, Francesca, Hauffman, Tom, Bjerg, Jesper Tataru, Skirtach, Andre G., Kochan, Kamila, McKee, Merrilyn, Wood, Bayden, Bedolla, Diana, Gianoncelli, Alessandra, Geerlings, Nicole M.J., Van Gerven, Nani, Remaut, Han, Geelhoed, Jeanine S., Millan-Solsona, Ruben, Fumagalli, Laura, Nielsen, Lars Peter, Franquet, Alexis, Manca, Jean V., Gomila, Gabriel, and Meysman, Filip J.R.

Published
2021

24. Cell Cycle, Filament Growth and Synchronized Cell Division in Multicellular Cable Bacteria

Author

Geochemistry, GeoLab Algemeen, Bio-, hydro-, and environmental geochemistry, Geerlings, Nicole M.J., Geelhoed, Jeanine S., Vasquez-Cardenas, Diana, Kienhuis, Michiel V.M., Hidalgo-Martinez, Silvia, Boschker, Henricus T.S., Middelburg, Jack J., Meysman, Filip J.R., Polerecky, Lubos, Geochemistry, GeoLab Algemeen, Bio-, hydro-, and environmental geochemistry, Geerlings, Nicole M.J., Geelhoed, Jeanine S., Vasquez-Cardenas, Diana, Kienhuis, Michiel V.M., Hidalgo-Martinez, Silvia, Boschker, Henricus T.S., Middelburg, Jack J., Meysman, Filip J.R., and Polerecky, Lubos

Published
2021

31. Predicted tortuosity of muds

Author

Boudreau, Bernard P. and Meysman, Filip J.R.

Subjects
Mud -- Structure, Mud -- Analysis, Porosity -- Analysis, Earth sciences
Abstract

Tortuosity figures prominently in geochemical, hydrological, and geophysical calculations concerned with sediments, but it is a difficult parameter to measure. Past theoretical models for predicting the tortuosity from porosity data do not work with marine muds, and scientists and engineers have had to resort to entirely empirical models, without a mechanistic explanation and with unknown predictive power. We offer the first geometric model for the dependence of tortuosity on porosity in marine muds; the model is based on the tortuosity of separated layers of nonoverlapping disks. The fitted geometric constant in this model indicates that natural marine sediments act as if their fabric were made of disks with thickness:diameter ratios very close to 1:2, which indicates a blocklike fabric with respect to diffusion. The model was also applied to predict the tortuosity of a variety of sediments and soils not in the original database, and it provides a satisfactory prediction of the mean trend in these data. Keywords: tortuosity, porosity, mud, modeling.

Published
2006

32. Bioirrigation in permeable sediments: advective pore-water transport induced by burrow ventilation

Author

Meysman, Filip J.R., Galaktionov, Oleksiy S., Gribsholt, Britta, and Middelburg, Jack J.

Subjects
Soil permeability -- Environmental aspects, Irrigation -- Environmental aspects, Sediments (Geology) -- Environmental aspects, Earth sciences
Abstract

The physical mechanism that drives bioirrigation is strongly dependent on the permeability of the sediment. We advance two mechanisms, each described by a corresponding microenvironment model. In muds, burrow water cannot penetrate the sediment, so bioirrigation is intrinsically driven by diffusional transfer across the burrow wall. This 'diffusive' mode of bioirrigation is accurately described by the classical tube irrigation model. In sands, ventilation flows can penetrate the surrounding sediment via dead end burrows. To quantify this 'advective' mode of bioirrigation, we propose a novel two-dimensional pocket injection model. This model's principal features are that (1) organisms indent the sediment-water interface with burrow structures, (2) the specific structure of the burrow can be neglected except for the location of a feeding pocket, and (3) burrow water is injected from this feeding pocket into the surrounding sediment. We tested the adequacy of the pocket injection model in a detailed case study of the lugworm Arenicola marina, comparing model simulations and experimental data from core incubations. Simulation of two different sets of inert tracer experiments shows good agreement between model and data, indicating that our model captures the relevant aspects of lugworm bioirrigation in permeable sediments.

Published
2006

36. Phosphorus Cycling and Burial in Sediments of a Seasonally Hypoxic Marine Basin

Author

Sulu-Gambari, Fatimah, Hagens, Mathilde, Behrends, Thilo, Seitaj, Dorina, Meysman, Filip J.R., Middelburg, Jack, Slomp, Caroline P., General geochemistry, Geochemistry, General geochemistry, and Geochemistry

Subjects
010504 meteorology & atmospheric sciences, Aquatic Science, Structural basin, Benthic flux, 010502 geochemistry & geophysics, 01 natural sciences, chemistry.chemical_compound, Pore water pressure, Cable bacteria, Recycling, 14. Life underwater, Ecology, Evolution, Behavior and Systematics, 0105 earth and related environmental sciences, Burial efficiency, Ecology, Sediment, Hypoxia (environmental), Phosphorus, Authigenic, Phosphate, 6. Clean water, Oceanography, chemistry, Environmental science, Sedimentary rock, Surface water
Abstract

Recycling of phosphorus (P) from sediments contributes to the development of bottom-water hypoxia in many coastal systems. Here, we present results of a year-long assessment of P dynamics in sediments of a seasonally hypoxic coastal marine basin (Lake Grevelingen, the Netherlands) in 2012. Sequential phosphorus extractions (SEDEX) and X-ray absorption spectroscopy (XAS) indicate that P was adsorbed to Fe-(III)-(oxyhydr)oxides when cable bacteria were active in the surface sediments in spring. With the onset of summer hypoxia, sulphide-induced dissolution of the Fe-(III)-(oxyhydr)oxides led to P release to the pore water and overlying water. The similarity in authigenic Ca-P concentrations in the sediment and suspended matter suggest that Ca-P is not formed in situ. The P burial efficiency was ≤ 32%. Hypoxia-driven sedimentary P recycling had a major impact on the water-column chemistry in the basin in 2012. Water-column monitoring data indicate up to ninefold higher surface water concentrations of phosphate in the basin in the late 1970s and a stronger hypoxia-driven seasonal P release from the sediment. The amplified release of P from the sediment in the past is attributed to the presence of a larger pool of Fe-bound P in the basin prior to the first onset of hypoxia. Given that P is not limiting, primary production in the basin has not been affected by the decadal changes in P availability and recycling over the past 40 years. The changes in P dynamics on decadal time scales were not recorded in sediment profiles of total P or organic C/total P.

Published
2017
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38. Abundance and Biogeochemical Impact of Cable Bacteria in Baltic Sea Sediments

Author

Hermans, Martijn, Lenstra, Wytze K., Hidalgo-Martinez, Silvia, van Helmond, Niels A.G.M., Witbaard, Rob, Meysman, Filip J.R., Gonzalez, Santiago, Slomp, Caroline P., Geochemistry, General geochemistry, Geochemistry, and General geochemistry

Subjects
Baltic States, Biogeochemical cycle, Geologic Sediments, Sulfide, Chemistry(all), 010501 environmental sciences, Sulfides, 01 natural sciences, chemistry.chemical_compound, Nitrate, Environmental Chemistry, 14. Life underwater, Sulfate, Biology, Finland, 0105 earth and related environmental sciences, Total organic carbon, chemistry.chemical_classification, Bacteria, Sediment, General Chemistry, Anoxic waters, Chemistry, chemistry, Environmental chemistry, Environmental science, Eutrophication
Abstract

[Image: see text] Oxygen depletion in coastal waters may lead to release of toxic sulfide from sediments. Cable bacteria can limit sulfide release by promoting iron oxide formation in sediments. Currently, it is unknown how widespread this phenomenon is. Here, we assess the abundance, activity, and biogeochemical impact of cable bacteria at 12 Baltic Sea sites. Cable bacteria were mostly absent in sediments overlain by anoxic and sulfidic bottom waters, emphasizing their dependence on oxygen or nitrate as electron acceptors. At sites that were temporarily reoxygenated, cable bacterial densities were low. At seasonally hypoxic sites, cable bacterial densities correlated linearly with the supply of sulfide. The highest densities were observed at Gulf of Finland sites with high rates of sulfate reduction. Microelectrode profiles of sulfide, oxygen, and pH indicated low or no in situ cable bacteria activity at all sites. Reactivation occurred within 5 days upon incubation of an intact sediment core from the Gulf of Finland with aerated overlying water. We found no relationship between cable bacterial densities and macrofaunal abundances, salinity, or sediment organic carbon. Our geochemical data suggest that cable bacteria promote conversion of iron monosulfides to iron oxides in the Gulf of Finland in spring, possibly explaining why bottom waters in this highly eutrophic region rarely contain sulfide in summer.

Published
2019

39. Abundance and Biogeochemical Impact of Cable Bacteria in Baltic Sea Sediments

Author

Geochemistry, General geochemistry, Hermans, Martijn, Lenstra, Wytze K., Hidalgo-Martinez, Silvia, van Helmond, Niels A.G.M., Witbaard, Rob, Meysman, Filip J.R., Gonzalez, Santiago, Slomp, Caroline P., Geochemistry, General geochemistry, Hermans, Martijn, Lenstra, Wytze K., Hidalgo-Martinez, Silvia, van Helmond, Niels A.G.M., Witbaard, Rob, Meysman, Filip J.R., Gonzalez, Santiago, and Slomp, Caroline P.

Published
2019

40. Mn/Ca ratios of Ammonia tepida as a proxy for seasonal coastal hypoxia

Author

General geochemistry, Geochemistry, Petersen, Jassin, Barras, Christine, Bézos, Antoine, La, Carole, Slomp, Caroline P., Meysman, Filip J.R., Mouret, Aurélia, Jorissen, Frans J., General geochemistry, Geochemistry, Petersen, Jassin, Barras, Christine, Bézos, Antoine, La, Carole, Slomp, Caroline P., Meysman, Filip J.R., Mouret, Aurélia, and Jorissen, Frans J.

Published
2019

43. Mn/Ca intra- and inter-test variability in the benthic foraminifer Ammonia tepida

Author

Petersen, Jassin, Barras, Christine, Bézos, Antoine, La, Carole, de Nooijer, Lennart J., Meysman, Filip J.R., Mouret, Aurélia, Slomp, Caroline P., Jorissen, Frans J., Geochemistry, and General geochemistry

Abstract

The adaptation of some benthic foraminiferal species to low-oxygen conditions provides the prospect of using the chemical composition of their tests as proxies for bottom water oxygenation. Manganese may be particularly suitable as such a geochemical proxy because this redox element is soluble in reduced form (Mn2+) and hence can be incorporated into benthic foraminiferal tests under low-oxygen conditions. Therefore, intra- and inter-test differences in foraminiferal Mn∕Ca ratios may hold important information about short-term variability in pore water Mn2+ concentrations and sediment redox conditions. Here, we studied Mn∕Ca intra- and inter-test variability in living individuals of the shallow infaunal foraminifer Ammonia tepida sampled in Lake Grevelingen (the Netherlands) in three different months of 2012. The deeper parts of this lake are characterized by seasonal hypoxia/anoxia with associated shifts in microbial activity and sediment geochemistry, leading to seasonal Mn2+ accumulation in the pore water. Earlier laboratory experiments with similar seawater Mn2+ concentrations as encountered in the pore waters of Lake Grevelingen suggest that intra-test variability due to ontogenetic trends (i.e. size-related effects) and/or other vital effects occurring during calcification in A. tepida (11–25 % relative SD, RSD) is responsible for part of the observed variability in Mn∕Ca. Our present results show that the seasonally highly dynamic environmental conditions in the study area lead to a strongly increased Mn∕Ca intra- and inter-test variability (average of 45 % RSD). Within single specimens, both increasing and decreasing trends in Mn∕Ca ratios with size are observed. Our results suggest that the variability in successive single-chamber Mn∕Ca ratios reflects the temporal variability in pore water Mn2+. Additionally, active or passive migration of the foraminifera in the surface sediment may explain part of the observed Mn∕Ca variability.

Published
2018

44. Characterization of the conductive structures in the periplasm of cable bacteria using combined TOF-SIMS/AFM

Author

Thiruvallur Eachambadi, Raghavendran, Boschker, Henricus T.S., Spampinato, Valentina, Franquet, Alexis, Hidalgo-Martinez, Silvia, Meysman, Filip J.R., and Manca, Jean V.

Subjects
cable bacteria, desulfobulbacae, TOF SIMS, atomic force microscopy
Abstract

Filamentous cable bacteria were recently discovered in marine sediments and are capable of transporting electrons inside their body over centimeter-scale distances [1]. This length scale of electron transport is more than three orders of magnitude greater than previously known in biology [2]. Identifying the conductive structures and the mechanism of this long-distance electron transfer will not only expand our knowledge of the role of cable bacteria in marine environments, but also could lead to novel applications in bioelectronics and microbial fuel cells. Recently, it was discovered shown that conductive structures are located in the cell envelope of cable bacteria. In this study, this conductive fiber envelope was extracted from cable bacteria, and TOF-SIMS was used to characterize the extracted material. TOF-SIMS was operated in the dual beam acquisition mode, where the Argon Gas Cluster Ion Beam (GCIB) was used as the sputter beam and Bismuth (Bi3) was used as the analysis beam. An in-situ AFM in contact mode was used to calibrate sputtering depths and to identify the positions of the layers. TOF-SIMS indicated that the fiber envelope is first made of a layer of protein followed by a carbohydrate layer. Based on the TOF-SIMS results, we will present a model where the conductive fibers are made of protein core, which are held together by a sheet of polysaccharide, most likely in the form of peptidoglycan. Proteomics would be the logical next step to further identify the proteins and sugars and their role in electron conductivity. TOF-SIMS analysis was financially supported by the HERCULES foundation. FWO, Hercules foundation

Published
2018

47. Mn/Ca intra- and inter-test variability in the benthic foraminifer Ammonia tepida

Author

Geochemistry, General geochemistry, Petersen, Jassin, Barras, Christine, Bézos, Antoine, La, Carole, de Nooijer, Lennart J., Meysman, Filip J.R., Mouret, Aurélia, Slomp, Caroline P., Jorissen, Frans J., Geochemistry, General geochemistry, Petersen, Jassin, Barras, Christine, Bézos, Antoine, La, Carole, de Nooijer, Lennart J., Meysman, Filip J.R., Mouret, Aurélia, Slomp, Caroline P., and Jorissen, Frans J.

Published
2018

48. Phosphorus Cycling and Burial in Sediments of a Seasonally Hypoxic Marine Basin

Author

General geochemistry, Geochemistry, Sulu-Gambari, Fatimah, Hagens, Mathilde, Behrends, Thilo, Seitaj, Dorina, Meysman, Filip J.R., Middelburg, Jack, Slomp, Caroline P., General geochemistry, Geochemistry, Sulu-Gambari, Fatimah, Hagens, Mathilde, Behrends, Thilo, Seitaj, Dorina, Meysman, Filip J.R., Middelburg, Jack, and Slomp, Caroline P.

Published
2018

49. Sedimentary oxygen dynamics in a seasonally hypoxic basin

Author

Seitaj, Dorina, Sulu-Gambari, Fatimah, Burdorf, Laurine D. W., Romero-Ramirez, Alicia, Maire, Olivier, Malkin, Sairah Y., Slomp, Caroline P., Meysman, Filip J.R., NWO-DARWIN: Dynamics of coastal hypoxia: an experimental study of sediment ecosystem recovery from anoxia, Geochemistry, and General geochemistry

Abstract

Seasonal hypoxia refers to the oxygen depletion that occurs in summer in the bottom water of stratified systems, and is increasingly observed in coastal areas worldwide. The process induces a seasonal cycle on the biogeochemistry of the underlying sediments, which remains poorly quantified. Here, we investigated the sedimentary oxygen consumption within Lake Grevelingen (The Netherlands), a saline coastal reservoir that is impacted by yearly recurrent bottom water hypoxia. Monthly sampling campaigns were conducted throughout 2012 at three sites along a depth gradient. Macrofauna sampling and sediment profile imaging demonstrated how summer hypoxia strongly impacts the benthic communities below 15 m of water depth. Benthic fluxes of oxygen, dissolved inorganic carbon, total alkalinity, and ammonium were determined by closed core incubations, while oxygen depth profiles were recorded by microsensor profiling of sediment cores. Our results reveal a pronounced seasonality in the sedimentary oxygen consumption. Low uptake rates in summer were caused by oxygen limitation, and resulted in the build-up of an “oxygen debt” through the accumulation of reduced iron sulfides. Highest oxygen uptake rates were recorded in fall, linked to the reoxidation of the pool of iron sulfides in the top layer. However, uptake rates remained unexpectedly high during winter and early spring, likely associated with the oxidation of iron sulfides down to centimeters depth due to the electrogenic sulfur oxidation by cable bacteria. Overall, our results suggest that the sedimentary oxygen dynamic in seasonally hypoxic coastal systems is characterized by a strongly amplified “oxygen debt” dynamics induced by cable bacteria.

Published
2017

50. Molybdenum dynamics in sediments of a seasonally-hypoxic coastal marine basin

Author

General geochemistry, Geochemistry, Sulu-Gambari, Fatimah, Roepert, Anne, Jilbert, Tom, Hagens, Mathilde, Meysman, Filip J.R., Slomp, Caroline P., General geochemistry, Geochemistry, Sulu-Gambari, Fatimah, Roepert, Anne, Jilbert, Tom, Hagens, Mathilde, Meysman, Filip J.R., and Slomp, Caroline P.

Published
2017

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