Polyphosphate Dynamics in Cable Bacteria

Abstract

Cable bacteria are multicellular sulfide oxidizing bacteria that display a unique metabolism based on long-distance electron transport. Cells in deeper sediment layers perform the sulfide oxidizing half-reaction whereas cells in the surface layers of the sediment perform the oxygen-reducing half-reaction. These half-reactions are coupled via electron transport through a conductive fiber network that runs along the shared cell envelope. Remarkably, only the sulfide oxidizing half-reaction is coupled to biosynthesis and growth whereas the oxygen reducing half-reaction serves to rapidly remove electrons from the conductive fiber network and is not coupled to energy generation and growth. Cells residing in the oxic zone are believed to (temporarily) rely on storage compounds of which polyphosphate (poly-P) is prominently present in cable bacteria. Here we investigate the role of poly-P in the metabolism of cable bacteria within the different redox environments. To this end, we combined nanoscale secondary ion mass spectrometry with dual-stable isotope probing (13C-DIC and 18O-H2O) to visualize the relationship between growth in the cytoplasm (13C-enrichment) and poly-P activity (18O-enrichment). We found that poly-P was synthesized in almost all cells, as indicated by 18O enrichment of poly-P granules. Hence, poly-P must have an important function in the metabolism of cable bacteria. Within the oxic zone of the sediment, where little growth is observed, 18O enrichment in poly-P granules was significantly lower than in the suboxic zone. Thus, both growth and poly-P metabolism appear to be correlated to the redox environment. However, the poly-P metabolism is not coupled to growth in cable bacteria, as many filaments from the suboxic zone showed poly-P activity but did not grow. We hypothesize that within the oxic zone, poly-P is used to protect the cells against oxidative stress and/or as a resource to support motility, while within the suboxic zone, poly-P is involved in the metabolic regulation before cells enter a non-growing stage.

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

“…Occasionally, an intense peak was observed at 971 cm −1 , as seen in the orange (633 nm) spectrum. This peak likely originates from phosphate stretching (Frost et al, 2016;Nkebiwe et al, 2022) in the polyphosphate granules that are widely present in cable bacteria (Sulu-Gambari et al, 2016a;Geerlings et al, 2022). However, such polyphosphate granules are not present in every cell (Geerlings et al, 2022), explaining the occasional presence of the 971 cm −1 peak in the spectra.…”

“…This peak likely originates from phosphate stretching (Frost et al, 2016;Nkebiwe et al, 2022) in the polyphosphate granules that are widely present in cable bacteria (Sulu-Gambari et al, 2016a;Geerlings et al, 2022). However, such polyphosphate granules are not present in every cell (Geerlings et al, 2022), explaining the occasional presence of the 971 cm −1 peak in the spectra. A complete annotation list of the Raman spectrum of native cable bacteria is provided in Supplementary Table 1.…”

“…This indicates that polyphosphate granules were occasionally present in cable bacterium cells. Polyphosphate granules are produced as a form of energy storage by active cable bacterium cells with access to sulfide, and are consumed to power the basal metabolism when cells reside in the oxygen-rich, sulfide-free top layer of the sediment (Sulu-Gambari et al, 2016b;Geerlings et al, 2022). Since cable bacterium filaments were mostly harvested from the oxic top layer of the sediment, polyphosphate granules were only sporadically detected.…”