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Cable Bacteria, Living Electrical Conduits in the Microbial World COMMENTARY Andreas Teskea,1

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Cable Bacteria, Living Electrical Conduits in the Microbial World COMMENTARY Andreas Teskea,1 COMMENTARY Cable bacteria, living electrical conduits in the microbial world COMMENTARY Andreas Teskea,1 Microorganisms spend their lives searching for chemical reactants that yield metabolically usable energy, one reactant providing electrons and the other accepting them in a redox reaction. In PNAS, Kjeldsen et al. (1) provide a comprehensive genomic and physiological analysis of bacteria that have evolved an ingenious solu- tion to the persistent problem that suitable reactants often do not occur together: They electrify their sedimentary habitat as living wires and connect redox couples over centimeters, vast distances in the microbial world. In aquatic sediments, microorganisms degrade and oxidize organic matter that settles on the sediment surface, using locally available electron acceptors in the sequence of their metabolic energy yield: Oxygen is consumed first, followed by nitrate, metal cations, and then sulfate, the dominant electron acceptor for anaer- Fig. 1. Microscopic images of cable bacteria. (A) Cable bacteria filaments oriented “ ” – obic metabolism in marine sediments. Sulfate reduction on a glass slide as living wires, aligned within a sulfide oxygen gradient. Image courtesy of Steffen Larsen and Lars R. Damgaard (Aarhus University, Aarhus, produces sulfide, which can be oxidized by diverse Denmark). (B) Scanning electron micrograph of cable bacterial cells from the microorganisms as soon as it overlaps with suitable Hudson River. Image courtesy of Yuri Gorby and Anne Hynes (Rensselaer oxidants, such as oxygen or nitrate (2). However, sulfide Polytechnic Institute, Troy, NY). (C) Cable bacteria stained with toluidine blue to is frequently consumed anaerobically within the sedi- visualize polyphosphates, a possible energy source for cathodic cells. Image ment, for example by abiotic reactions with metals, be- courtesy of Lars Peter Nielsen (Aarhus University, Aarhus, Denmark). fore it diffuses to the surface where oxygen and nitrate are available. Microbes have developed strategies to from O2 at the sediment surface co-occurs with sulfide tap into this potential energy source regardless. The disappearance in deeper anoxic sediment layers. Oxy- large filamentous bacterium Thioploca shuttles up and gen and sulfide dynamics respond faster than molecular down between sulfidic sediment layers and overlying diffusion across the gap would allow (4). The ensuing waters, bridging the gap by transporting its preferred search for long-distance electron transporters yielded electron acceptor nitrate into the sulfidic sediment (3). multicelled bacterial filaments vertically embedded in These biological sulfide sinks have obvious ecological sediments; slicing horizontally through the sediment relevance for the health of aquatic environments. interrupted the electron flow (5). The filaments—aptly Other than transporting the partners of an energy- named cable bacteria (Fig. 1A)—were covered by nu- yielding redox reaction, or waiting for physical distur- merous parallel fibers in the periplasmic space, run- bance to mix electron donors and acceptors, how could ning along the length of the filament. These fibers, microbes exchange electrons between spatially sepa- sandwiched between the cell membrane below and rated reactants? A biological cable would be required the cell envelope above, have significant charge stor- to transport electrical charges, while avoiding charge age capacity (5). The fibers give each cable bacterial dissipation into the surrounding wet sediments, and cell the look of an extended barrel covered with outpacing diffusion or abiotic reactions of the redox ridges, resembling the ribbed trunk of a saguaro cac- partners. Microelectrode profiling of marine sediments tus (5, 6) (Fig. 1B). showed that such cables indeed exist (4). A localized Cable bacteria have a strong affinity to sulfide and − peak of proton consumption due to OH production deplete its in situ concentration below 1 μM (7). As aDepartment of Marine Sciences, The University of North Carolina at Chapel Hill, Chapel Hill, NC 27599 Author contributions: A.T. wrote the paper. The author declares no conflict of interest. Published under the PNAS license. See companion article on page 19116. 1Email: [email protected]. Published online September 9, 2019. www.pnas.org/cgi/doi/10.1073/pnas.1913413116 PNAS | September 17, 2019 | vol. 116 | no. 38 | 18759–18761 Downloaded by guest on September 26, 2021 they grow from a near-surface inoculum into the sediment, they ex- In aerobic bacteria, terminal oxidases transfer electrons tend the sulfide-free zone several centimeters deeper into the from the membrane quinol pool to oxygen, creating the mem- sediment while consuming oxygen within the upper 1 to 2 mm brane potential for chemiosmotic energy conservation. Cable (8). Although these bacteria function as aerobic sulfide oxidizers, bacteria lack a complete membrane-bound terminal oxidase they are unrelated to previously investigated filamentous sulfide for aerobic respiration. Instead, periplasmatic oxidases may oxidizers, including Thioploca, within the Gammaproteobacteria transfer electrons from the conductive cable to oxygen, or use (9). Gene-based phylogeny placed the cable bacterial clade— a novel cytochrome–hemoglobin fusion protein for this pur- presently containing 2 proposed candidate genera, Candidatus pose, but bypass chemiosmotic energy conservation. Since Electrothrix and Candidatus Electronema—into the Desulfobulba- bacteria excel in conserving metabolic energy even from ceae, a sulfate-reducing bacterial family within the class Deltapro- barely exergonic reactions, why would cable bacteria “flare teobacteria (10). Therefore, the genomic and physiological off” the electron stream, almost like a gas flare during petroleum blueprint of the cable bacteria might share notable features with production? Since oxygen barely penetrates organic-rich sedi- their deltaproteobacterial cousins. ments, the oxygen-exposed cathodic region of a cable bacte- These observations provide the starting point for the compre- rium filament is shorter than the wider anodic region where hensive study of cable bacteria physiology and evolution by Kjeldsen et al. (1) in PNAS. By examining genomes, metapro- Kjeldsen et al. show that cable bacteria filaments teomes, and microscopic observations of cable bacteria, they assume different biogeochemical and have untangled key pathways, physiological strategies, and evolutionary linkages that define the cable bacteria and their physiological roles that are reminiscent of unique adaptations that enable them to thrive as living wires per- functional specialization within an organism forming long-distance electron transport in their sedimentary niche (Fig. 1). While cable bacteria are in some ways character- that is well adapted to its sedimentary habitat. ized by gradual modification of physiological and genomic fea- tures within the Desulfobulbaceae, in other ways they have no sulfide oxidation takes place, resulting in a bottleneck of high known counterparts and constitute genuine terra incognita in electron flow at the cathodic end. This constraint may have fine- the microbial world. tuned oxygen reduction for speed while completely jettisoning Starting with recognizable features, cable bacteria have aerobic, chemiosmotic energy generation. Considering the repurposed the canonical pathway of reduction of sulfate to physiological stress caused by reactive oxygen species, fully sulfide (11) and run it into the oxidative direction. Metabolic en- aerobic energy metabolism may not be sustainable anyway; for ergy would be generated chemiosmotically by membrane trans- example, sulfate-reducing bacteria of the genus Desulfovibrio fer of electrons derived from sulfide oxidation, and by substrate- can respire aerobically but do not sustain growth (16, 17). Since level phosphorylation in the terminal step of sulfate release. oxygen-exposed cable bacteria reveal physiological stress by Within the Desulfobulbaceae, the sulfide-oxidizing bacterium reduced protein biosynthesis activity (18), it makes sense for Desulfurivibrio alkaliphilus uses a similar metabolic strategy and cable bacteria to “switch out” their oxygen-impacted ends by harbors genes and specific enzymatic steps—in particular of the moving in loops when encountering oxygen, a pattern that avoids initial reactions that oxidize sulfide to polysulfide and elemental and in part reverses extensive oxygen exposure (19). Sulfide oxida- sulfur—that provide models for the sulfide-oxidizing metabolism tion with nitrate and nitrite could avoid oxygen toxicity (20), but this of the cable bacteria (12). The production of elemental sulfur possibility remains to be investigated more closely. would also allow subsequent sulfur disproportionation to sulfide Similar to many autotrophic sulfate-reducing bacteria, cable and sulfate, a widely shared physiological capability among the bacteria perform carbon fixation via the energetically effi- Desulfobulbaceae (2). cient Wood–Ljungdahl pathway, while supplementing autotro- Electrons gained by sulfide oxidation can be shuttled from the phy by heterotrophic carbon assimilation. To varying degrees, quinone pool in the periplasmatic membrane to the electrically cable bacteria can assimilate low-molecular-weight carbon sources conductive cables by periplasmatic c-type cytochromes, like those such as acetate and propionate; the latter is a characteris- in the metal- and sulfur-reducing bacterial genera Shewanella tic substrate of many Desulfobulbaceae
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