Cable bacteria have acquired a unique metabolism, which induces long-distance electron transport along their centimeter-long multicellular filaments. At present, cable bacteria are thought to form a monophyletic clade with two described genera. However, their diversity has not been systematically investigated. To investigate the phylogenetic relationships within the cable bacteria clade, 16S rRNA gene sequences were compiled from literature and public databases (SILVA 138 SSU and NCBI GenBank). These were complemented with novel sequences obtained from natural sediment enrichments across a wide range of salinities (2–34). To enable taxonomic resolution at the species level, we designed a procedure to attain full-length 16S rRNA gene sequences from individual cable bacterium filaments using an optimized nested PCR protocol and Sanger sequencing. The final database contained 1,876 long 16S rRNA gene sequences (≥800 bp) originating from 92 aquatic locations, ranging from polar to tropical regions and from intertidal to deep sea sediments. The resulting phylogenetic tree reveals 90 potential species-level clades (based on a delineation value of 98.7% 16S rRNA gene sequence identity) that reside within six genus-level clusters. Hence, the diversity of cable bacteria appears to be substantially larger than the two genera and 13 species that have been officially named up to now. Particularly brackish environments with strong salinity fluctuations, as well as sediments with low free sulfide concentrations and deep sea sediments harbor a large pool of novel and undescribed cable bacteria taxa.@en

Cable bacteria can reach high densities in coastal sediments, and as a result of their unusual electrogenic lifestyle and intense metabolic activity, exert a major and distinct impact on biogeochemical cycling, both locally in sediments and at the ecosystem level. This appears to be particularly true for seasonally hypoxic systems, but the driving force behind the proliferation of cable bacteria in these systems is not well understood. Moreover, the metabolism of cable bacteria induces strong acid production, which can be buffered through carbonate dissolution in sediments. A strong depletion of alkalinity in the pore water is therefore expected in carbonate-poor sediments. To evaluate the impact of cable bacteria metabolism on sediment geochemistry, we performed field sampling and laboratory sediment incubations in two seasonally hypoxic sites: one carbonate-poor site with low levels of free sulfide in pore water (Yarra Estuary, Australia) and one carbonate-rich site with high free sulfide (Lake Grevelingen, The Netherlands). Active cable bacteria populations were found in both field locations, with higher abundance and activity observed in spring compared to autumn. The sediment incubations tracked the metabolic activity of cable bacteria over time (maximum 84 days), and confirmed the fast development of an electric network (cell doubling time: ∼19 h). These results suggest that cable bacteria are widespread in seasonally hypoxic systems, supporting previous findings. Cable bacteria acidified the sediment by > 1.5 pH units in 6–13 days (differing per site) and their activity accounted for >70% of the oxygen uptake. A clear subsurface accumulation of Fe²⁺ was observed after 8 days of Yarra sediment incubations, indicative of increased FeS dissolution as e-SOx developed. The increased availability of sulfide from FeS dissolution promotes a positive-feedback loop that we infer allowed for a faster development of cable bacteria in the carbonate-poor sediments. A depletion of total alkalinity was observed in the deeper Yarra sediment, whereas, a higher alkalinity efflux was previously observed in the carbonate-rich sediments from Lake Grevelingen. These results suggest a differential pH and alkalinity dynamic due to the interaction between the local carbonate content of the sediment and cable bacteria activity.

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