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

Nicole M J Geerlings,Henricus T S Boschker,Diana Vasquez-Cardenas,Lubos Polerecky,Jeanine S Geelhoed,Filip J R Meysman,Michiel V M Kienhuis,Jack J Middelburg,Silvia Hidalgo-Martinez

doi:10.3389/fmicb.2021.620807

Nicole M J Geerlings, Henricus T S Boschker + Show 7 more

Open Access

https://doi.org/10.3389/fmicb.2021.620807

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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.

Highlights

Cable bacteria are multicellular, filamentous bacteria that gain metabolic energy by coupling the oxidation of sulfide (H2S + 4 H2O → SO42− + 8 e− + 10 H+) in deeper sediment layers to the reduction of oxygen (O2 + 4 H+ + 4 e− → 2 H2O) at the sediment-water interface (Nielsen et al, 2010; Pfeffer et al, 2012)
Combining duallabel 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
Our data reveals that the cell cycle of cable bacteria is highly similar to that of the Gram-negative model bacterium E. coli

Summary

Introduction

Filamentous bacteria that gain metabolic energy by coupling the oxidation of sulfide (H2S + 4 H2O → SO42− + 8 e− + 10 H+) in deeper sediment layers to the reduction of oxygen (O2 + 4 H+ + 4 e− → 2 H2O) at the sediment-water interface (Nielsen et al, 2010; Pfeffer et al, 2012). The necessary electrical coupling between these two redox half reactions is ensured by the transport of electrons over centimeter-scale distances through a regularly spaced network of highly conductive fibers that run along the whole filament (Meysman et al, 2019; Thiruvallur Eachambadi et al, 2020). Cell Division in Cable Bacteria a wider range of sediment depths, which gives them a competitive advantage over other, single-celled sulfide-oxidizing bacteria (Meysman, 2018) Since their discovery, cable bacteria have been found at the oxic-anoxic interface in a wide range of aquatic sediment environments, including marine (e.g., Malkin et al, 2014; Burdorf et al, 2017), freshwater (Risgaard-Petersen et al, 2015), and aquifer (Müller et al, 2016) sediments. Cable bacteria have been found attached to the anode of a benthic microbial fuel cell placed in anaerobic conditions (Reimers et al, 2017) or in association with oxygenated zones around plant roots (Scholz et al, 2019) and worm tubes in marine sediments (Aller et al, 2019)

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