Microbial carbon metabolism associated with electrogenic sulphur oxidation in coastal sediments

Abstract

Recently, a novel electrogenic type of sulphur oxidation was documented in marine sediments, whereby filamentous cable bacteria (Desulfobulbaceae) are mediating electron transport over cm-scale distances. These cable bacteria are capable of developing an extensive network within days, implying a highly efficient carbon acquisition strategy. Presently, the carbon metabolism of cable bacteria is unknown, and hence we adopted a multidisciplinary approach to study the carbon substrate utilization of both cable bacteria and associated microbial community in sediment incubations. Fluorescence in situ hybridization showed rapid downward growth of cable bacteria, concomitant with high rates of electrogenic sulphur oxidation, as quantified by microelectrode profiling. We studied heterotrophy and autotrophy by following 13C-propionate and -bicarbonate incorporation into bacterial fatty acids. This biomarker analysis showed that propionate uptake was limited to fatty acid signatures typical for the genus Desulfobulbus. The nanoscale secondary ion mass spectrometry analysis confirmed heterotrophic rather than autotrophic growth of cable bacteria. Still, high bicarbonate uptake was observed in concert with the development of cable bacteria. Clone libraries of 16S complementary DNA showed numerous sequences associated to chemoautotrophic sulphur-oxidizing Epsilon- and Gammaproteobacteria, whereas 13C-bicarbonate biomarker labelling suggested that these sulphur-oxidizing bacteria were active far below the oxygen penetration. A targeted manipulation experiment demonstrated that chemoautotrophic carbon fixation was tightly linked to the heterotrophic activity of the cable bacteria down to cm depth. Overall, the results suggest that electrogenic sulphur oxidation is performed by a microbial consortium, consisting of chemoorganotrophic cable bacteria and chemolithoautotrophic Epsilon- and Gammaproteobacteria. The metabolic linkage between these two groups is presently unknown and needs further study.

Ecosystem metabolism in salt marsh tidal creeks and ponds : applying triple oxygen isotopes and other gas tracers to novel environments

“…The spatial and temporal decoupling of O2 removal from the water column and DIC efflux from the sediments by sulfate reducing cable bacteria could also affect apparent daytime GPPDIC/GPPO2 ratios. Over daylight periods with the largest O2 concentrations and thermodynamic drive for this reaction, O2 should be removed from the water column more rapidly than otherwise indicated from RO2, which was derived from dark, low O2 chambers; oxygen consuming cable bacteria have growth rates that are an order of magnitude slower under anoxic conditions than near O2 saturation (Vasquez-Cardenas et al 2015), suggesting a strong dependence on relative O2 availability. Meanwhile DIC release from the sediments is mediated by additional metabolisms and distance beneath the sediment-water interface, including extensive chemolithoautotrophy and DIC uptake in the microbial consortia associated with the cable bacteria activity (Vasquez-Cardenas et al 2015).…”

“…DIC uptake by Gamma-and Epsilon-proteobacteria in microbial consortia with cable bacteria (supplementary Fig. S1) have a very strong dependence on water column oxygen concentration (and its effects on cable bacteria activity), with DIC uptake by these proteobacteria 20 times slower under anoxic conditions than at 80% O2 saturation (0.02 versus 0.4 mmol DIC m -2 h -1 ; Vasquez-Cardenas et al 2015). Rates are likely stimulated even more as the water column O2 becomes highly supersaturated as in the pond at midday.…”

Impact of Seasonal Hypoxia on Activity and Community Structure of Chemolithoautotrophic Bacteria in a Coastal Sediment

“…The consequences of these three mechanisms on the chemolithoautotrophic community have, however, not been studied. The first sulfur-oxidizing mechanism has been shown to affect the chemolithoautotrophic community in sediments only under laboratory conditions (15), while the third mechanisms may directly involve chemolithoautotrophic Beggiatoaceae, as some species are known to grow autotrophically (16). Accordingly, we hypothesize that the presence of these sulfur oxidation regimes, as well as the depletion of O 2 and NO 3 Ϫ , will result in a strong seasonality in both the chemolithoautotrophic activity and community structure under natural conditions.…”

Electrically Conductive Pili from Pilin Genes of Phylogenetically Diverse Microorganisms

“…It has been proposed that cable bacteria accept electrons from sulfide-oxidizing bacteria via DIET (Vasquez-Cardenas et al 2015). Genome sequences of cable bacteria have yet to be published but a genome is available for Desulfurivibrio alkaliphilus (Melton et al 2016), which is closely related to some species of cable bacteria (Müller et al 2016).…”

“…18, 2017; with elemental sulfur/polysulfide as the electron acceptor (Sorokin et al 2008) and microorganisms capable of elemental sulfur/polysulfide reduction are often capable of electron transfer to Fe(III) or other extracellular electron acceptors (Lovley et al 2004). If cable bacteria closely related to D. alkaliphilus have similar pilin genes this might provide a mechanism for the proposed DIET between cable bacteria and sulfur oxidizers (Vasquez-Cardenas et al 2015). The fact that cable bacteria or their putative sulfuroxidizing partners are not available in pure culture currently limits further investigation into this possibility.…”