The Cell Envelope Structure of Cable Bacteria

Rob Cornelissen; Andreas Bøggild; Raghavendran Thiruvallur Eachambadi; Roman I. Koning; Anna Kremer; Silvia Hidalgo-Martinez; Eva Maria Zetsche; Lars R. Damgaard; Robin Bonné; Jeroen Drijkoningen; Jeanine S. Geelhoed; Thomas Boesen; Henricus T.S. Boschker; Roland Valcke; Lars Peter Nielsen; Jan D'Haen; Jean V. Manca; Filip J.R. Meysman

doi:10.3389/fmicb.2018.03044

The Cell Envelope Structure of Cable Bacteria

Rob Cornelissen, Andreas Bøggild, Raghavendran Thiruvallur Eachambadi, Roman I. Koning, Anna Kremer, Silvia Hidalgo-Martinez, Eva Maria Zetsche, Lars R. Damgaard, Robin Bonné, Jeroen Drijkoningen, Jeanine S. Geelhoed, Thomas Boesen, Henricus T.S. Boschker, Roland Valcke, Lars Peter Nielsen, Jan D'Haen, Jean V. Manca, Filip J.R. Meysman^*

^*Corresponding author af dette arbejde

Publikation: Bidrag til tidsskrift/Konferencebidrag i tidsskrift /Bidrag til avis › Tidsskriftartikel › Forskning › peer review

24 Citationer (Scopus)

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Abstract

Cable bacteria are long, multicellular micro-organisms that are capable of transporting electrons from cell to cell along the longitudinal axis of their centimeter-long filaments. The conductive structures that mediate this long-distance electron transport are thought to be located in the cell envelope. Therefore, this study examines in detail the architecture of the cell envelope of cable bacterium filaments through a combination of classical electron microscopy, cryo-based electron microscopy and tomography, focused ion beam-scanning electron microscopy and atomic force microscopy. We systematically imaged intact filaments with varying diameters. In addition, we investigated the periplasmic fiber sheath that remains after the cytoplasm and membranes have been removed by chemical extraction. Based on these investigations, we present a quantitative structural model of a cable bacterium. Cable bacteria build their cell envelope by a parallel concatenation of ridge compartments that have a standard size. Larger diameter filaments simply incorporate more parallel ridge compartments. Each ridge compartment contains a ~50 nm diameter fiber in the periplasmic space. These fibers are continuous across cell-to-cell junctions, which display a conspicuous cartwheel structure that is likely made by invaginations of the outer cell membrane around the periplasmic fibers. The continuity of the periplasmic fibers across cells makes them a prime candidate for the sought-after electron conducting structure in cable bacteria.

Originalsprog	Engelsk
Artikelnummer	3044
Tidsskrift	Frontiers in Microbiology
Vol/bind	9
Antal sider	13
ISSN	1664-302X
DOI	https://doi.org/10.3389/fmicb.2018.03044
Status	Udgivet - 20 dec. 2018

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10.3389/fmicb.2018.03044Licens: CC BY

fmicb-09-03044Forlagets udgivne version, 3,2 MBLicens: CC BY

https://www.frontiersin.org/article/10.3389/fmicb.2018.03044

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Cornelissen, R., Bøggild, A., Thiruvallur Eachambadi, R., Koning, R. I., Kremer, A., Hidalgo-Martinez, S., Zetsche, E. M., Damgaard, L. R., Bonné, R., Drijkoningen, J., Geelhoed, J. S., Boesen, T., Boschker, H. T. S., Valcke, R., Nielsen, L. P., D'Haen, J., Manca, J. V., & Meysman, F. J. R. (2018). The Cell Envelope Structure of Cable Bacteria. Frontiers in Microbiology, 9, Artikel 3044. https://doi.org/10.3389/fmicb.2018.03044

@article{6531bb49c19b47a6b1699412c160604a,

title = "The Cell Envelope Structure of Cable Bacteria",

abstract = "Cable bacteria are long, multicellular micro-organisms that are capable of transporting electrons from cell to cell along the longitudinal axis of their centimeter-long filaments. The conductive structures that mediate this long-distance electron transport are thought to be located in the cell envelope. Therefore, this study examines in detail the architecture of the cell envelope of cable bacterium filaments through a combination of classical electron microscopy, cryo-based electron microscopy and tomography, focused ion beam-scanning electron microscopy and atomic force microscopy. We systematically imaged intact filaments with varying diameters. In addition, we investigated the periplasmic fiber sheath that remains after the cytoplasm and membranes have been removed by chemical extraction. Based on these investigations, we present a quantitative structural model of a cable bacterium. Cable bacteria build their cell envelope by a parallel concatenation of ridge compartments that have a standard size. Larger diameter filaments simply incorporate more parallel ridge compartments. Each ridge compartment contains a ~50 nm diameter fiber in the periplasmic space. These fibers are continuous across cell-to-cell junctions, which display a conspicuous cartwheel structure that is likely made by invaginations of the outer cell membrane around the periplasmic fibers. The continuity of the periplasmic fibers across cells makes them a prime candidate for the sought-after electron conducting structure in cable bacteria.",

keywords = "atomic force microscopy, cable bacteria, cell envelope, electron microscopy, long-distance electron transfer, periplasmic fibers",

author = "Rob Cornelissen and Andreas B{\o}ggild and {Thiruvallur Eachambadi}, Raghavendran and Koning, {Roman I.} and Anna Kremer and Silvia Hidalgo-Martinez and Zetsche, {Eva Maria} and Damgaard, {Lars R.} and Robin Bonn{\'e} and Jeroen Drijkoningen and Geelhoed, {Jeanine S.} and Thomas Boesen and Boschker, {Henricus T.S.} and Roland Valcke and Nielsen, {Lars Peter} and Jan D'Haen and Manca, {Jean V.} and Meysman, {Filip J.R.}",

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Cornelissen, R, Bøggild, A, Thiruvallur Eachambadi, R, Koning, RI, Kremer, A, Hidalgo-Martinez, S, Zetsche, EM, Damgaard, LR, Bonné, R, Drijkoningen, J, Geelhoed, JS, Boesen, T, Boschker, HTS, Valcke, R, Nielsen, LP, D'Haen, J, Manca, JV & Meysman, FJR 2018, 'The Cell Envelope Structure of Cable Bacteria', Frontiers in Microbiology, bind 9, 3044. https://doi.org/10.3389/fmicb.2018.03044

TY - JOUR

T1 - The Cell Envelope Structure of Cable Bacteria

AU - Cornelissen, Rob

AU - Bøggild, Andreas

AU - Thiruvallur Eachambadi, Raghavendran

AU - Koning, Roman I.

AU - Kremer, Anna

AU - Hidalgo-Martinez, Silvia

AU - Zetsche, Eva Maria

AU - Damgaard, Lars R.

AU - Bonné, Robin

AU - Drijkoningen, Jeroen

AU - Geelhoed, Jeanine S.

AU - Boesen, Thomas

AU - Boschker, Henricus T.S.

AU - Valcke, Roland

AU - Nielsen, Lars Peter

AU - D'Haen, Jan

AU - Manca, Jean V.

AU - Meysman, Filip J.R.

PY - 2018/12/20

Y1 - 2018/12/20

N2 - Cable bacteria are long, multicellular micro-organisms that are capable of transporting electrons from cell to cell along the longitudinal axis of their centimeter-long filaments. The conductive structures that mediate this long-distance electron transport are thought to be located in the cell envelope. Therefore, this study examines in detail the architecture of the cell envelope of cable bacterium filaments through a combination of classical electron microscopy, cryo-based electron microscopy and tomography, focused ion beam-scanning electron microscopy and atomic force microscopy. We systematically imaged intact filaments with varying diameters. In addition, we investigated the periplasmic fiber sheath that remains after the cytoplasm and membranes have been removed by chemical extraction. Based on these investigations, we present a quantitative structural model of a cable bacterium. Cable bacteria build their cell envelope by a parallel concatenation of ridge compartments that have a standard size. Larger diameter filaments simply incorporate more parallel ridge compartments. Each ridge compartment contains a ~50 nm diameter fiber in the periplasmic space. These fibers are continuous across cell-to-cell junctions, which display a conspicuous cartwheel structure that is likely made by invaginations of the outer cell membrane around the periplasmic fibers. The continuity of the periplasmic fibers across cells makes them a prime candidate for the sought-after electron conducting structure in cable bacteria.

AB - Cable bacteria are long, multicellular micro-organisms that are capable of transporting electrons from cell to cell along the longitudinal axis of their centimeter-long filaments. The conductive structures that mediate this long-distance electron transport are thought to be located in the cell envelope. Therefore, this study examines in detail the architecture of the cell envelope of cable bacterium filaments through a combination of classical electron microscopy, cryo-based electron microscopy and tomography, focused ion beam-scanning electron microscopy and atomic force microscopy. We systematically imaged intact filaments with varying diameters. In addition, we investigated the periplasmic fiber sheath that remains after the cytoplasm and membranes have been removed by chemical extraction. Based on these investigations, we present a quantitative structural model of a cable bacterium. Cable bacteria build their cell envelope by a parallel concatenation of ridge compartments that have a standard size. Larger diameter filaments simply incorporate more parallel ridge compartments. Each ridge compartment contains a ~50 nm diameter fiber in the periplasmic space. These fibers are continuous across cell-to-cell junctions, which display a conspicuous cartwheel structure that is likely made by invaginations of the outer cell membrane around the periplasmic fibers. The continuity of the periplasmic fibers across cells makes them a prime candidate for the sought-after electron conducting structure in cable bacteria.

KW - atomic force microscopy

KW - cable bacteria

KW - cell envelope

KW - electron microscopy

KW - long-distance electron transfer

KW - periplasmic fibers

UR - http://www.scopus.com/inward/record.url?scp=85061577956&partnerID=8YFLogxK

U2 - 10.3389/fmicb.2018.03044

DO - 10.3389/fmicb.2018.03044

M3 - Journal article

C2 - 30619135

SN - 1664-302X

VL - 9

JO - Frontiers in Microbiology

JF - Frontiers in Microbiology

M1 - 3044

ER -

The Cell Envelope Structure of Cable Bacteria

Abstract

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