Comparative genomic analysis of nickel homeostasis in cable bacteria.

BACKGROUND: Cable bacteria are filamentous members of the Desulfobulbaceae family that are capable of performing centimetre­scale electron transport in marine and freshwater sediments. This long­distance electron transport is mediated by a network of parallel conductive fibres embedded in the cell envelope. This fibre network efficiently transports electrical currents along the entire length of the centimetre­long filament. Recent analyses show that these fibres consist of metalloproteins that harbour a novel nickel­containing cofactor, which indicates that cable bacteria have evolved a unique form of biological electron transport. This nickel­dependent conduction mechanism suggests that cable bacteria are strongly dependent on nickel as a biosynthetic resource. Here, we performed a comprehensive comparative genomic analysis of the genes linked to nickel homeostasis. We compared the genome­encoded adaptation to nickel of cable bacteria to related members of the Desulfobulbaceae family and other members of the Desulfobulbales order. RESULTS: Presently, four closed genomes are available for the monophyletic cable bacteria clade that consists of the genera Candidatus Electrothrix and Candidatus Electronema. To increase the phylogenomic coverage, we additionally generated two closed genomes of cable bacteria: Candidatus Electrothrix gigas strain HY10­6 and Candidatus Electrothrix antwerpensis strain GW3­4, which are the first closed genomes of their respective species. Nickel homeostasis genes were identified in a database of 38 cable bacteria genomes (including 6 closed genomes). Gene prevalence was compared to 19 genomes of related strains, residing within the Desulfobulbales order but outside of the cable bacteria clade, revealing several genome­encoded adaptations to nickel homeostasis in cable bacteria. Phylogenetic analysis indicates that nickel importers, nickel­binding enzymes and nickel chaperones of cable bacteria are affiliated to organisms outside the Desulfobulbaceae family, with several proteins showing affiliation to organisms outside of the Desulfobacterota phylum. Conspicuously, cable bacteria encode a unique periplasmic nickel export protein RcnA, which possesses a putative cytoplasmic histidine­rich loop that has been largely expanded compared to RcnA homologs in other organisms. CONCLUSION: Cable bacteria genomes show a clear genetic adaptation for nickel utilization when compared to closely related genera. This fully aligns with the nickel­dependent conduction mechanism that is uniquely found in cable bacteria.

Interaction of living cable bacteria with carbon electrodes in bioelectrochemical systems.

Cable bacteria are filamentous bacteria that couple the oxidation of sulfide in sediments to the reduction of oxygen via long-distance electron transport over centimeter distances through periplasmic wires. However, the capability of cable bacteria to perform extracellular electron transfer to acceptors, such as electrodes, has remained elusive. In this study, we demonstrate that living cable bacteria actively move toward electrodes in different bioelectrochemical systems. Carbon felt and carbon fiber electrodes poised at +200 mV attracted live cable bacteria from the sediment. When the applied potential was switched off, cable bacteria retracted from the electrode. qPCR and scanning electron microscopy corroborated this finding and revealed cable bacteria in higher abundance present on the electrode surface compared with unpoised controls. These experiments raise new possibilities to study metabolism of cable bacteria and cultivate them in bioelectrochemical devices for bioelectronic applications, such as biosensing and bioremediation. IMPORTANCE: Extracellular electron transfer is a metabolic function associated with electroactive bacteria wherein electrons are exchanged with external electron acceptors or donors. This feature has enabled the development of several applications, such as biosensing, carbon capture, and energy recovery. Cable bacteria are a unique class of long, filamentous microbes that perform long-distance electron transport in freshwater and marine sediments. In this study, we demonstrate the attraction of cable bacteria toward carbon electrodes and demonstrate their potential electroactivity. This finding enables electronic control and monitoring of the metabolism of cable bacteria and may, in turn, aid in the development of bioelectronic applications.

Cable Bacteria Skeletons as Catalytically Active Electrodes.

Cable bacteria are multicellular, filamentous bacteria that use internal conductive fibers to transfer electrons over centimeter distances from donors within anoxic sediment layers to oxygen at the surface. We extracted the fibers and used them as free-standing bio-based electrodes to investigate their electrocatalytic behavior. The fibers catalyzed the reversible interconversion of oxygen and water, and an electric current was running through the fibers even when the potential difference was generated solely by a gradient of oxygen concentration. Oxygen reduction as well as oxygen evolution were confirmed by optical measurements. Within living cable bacteria, oxygen reduction by direct electrocatalysis on the fibers and not by membrane-bound proteins readily explains exceptionally high cell-specific oxygen consumption rates observed in the oxic zone, while electrocatalytic water oxidation may provide oxygen to cells in the anoxic zone.

Division of labor and growth during electrical cooperation in multicellular cable bacteria.

Multicellularity is a key evolutionary innovation, leading to coordinated activity and resource sharing among cells, which generally occurs via the physical exchange of chemical compounds. However, filamentous cable bacteria display a unique metabolism in which redox transformations in distant cells are coupled via long-distance electron transport rather than an exchange of chemicals. This challenges our understanding of organismal functioning, as the link among electron transfer, metabolism, energy conservation, and filament growth in cable bacteria remains enigmatic. Here, we show that cells within individual filaments of cable bacteria display a remarkable dichotomy in biosynthesis that coincides with redox zonation. Nanoscale secondary ion mass spectrometry combined with 13C (bicarbonate and propionate) and 15N-ammonia isotope labeling reveals that cells performing sulfide oxidation in deeper anoxic horizons have a high assimilation rate, whereas cells performing oxygen reduction in the oxic zone show very little or no label uptake. Accordingly, oxygen reduction appears to merely function as a mechanism to quickly dispense of electrons with little to no energy conservation, while biosynthesis and growth are restricted to sulfide-respiring cells. Still, cells can immediately switch roles when redox conditions change, and show no differentiation, which suggests that the "community service" performed by the cells in the oxic zone is only temporary. Overall, our data reveal a division of labor and electrical cooperation among cells that has not been seen previously in multicellular organisms.

On the evolution and physiology of cable bacteria.

Cable bacteria of the family Desulfobulbaceae form centimeter-long filaments comprising thousands of cells. They occur worldwide in the surface of aquatic sediments, where they connect sulfide oxidation with oxygen or nitrate reduction via long-distance electron transport. In the absence of pure cultures, we used single-filament genomics and metagenomics to retrieve draft genomes of 3 marine Candidatus Electrothrix and 1 freshwater Ca. Electronema species. These genomes contain >50% unknown genes but still share their core genomic makeup with sulfate-reducing and sulfur-disproportionating Desulfobulbaceae, with few core genes lost and 212 unique genes (from 197 gene families) conserved among cable bacteria. Last common ancestor analysis indicates gene divergence and lateral gene transfer as equally important origins of these unique genes. With support from metaproteomics of a Ca. Electronema enrichment, the genomes suggest that cable bacteria oxidize sulfide by reversing the canonical sulfate reduction pathway and fix CO2 using the Wood-Ljungdahl pathway. Cable bacteria show limited organotrophic potential, may assimilate smaller organic acids and alcohols, fix N2, and synthesize polyphosphates and polyglucose as storage compounds; several of these traits were confirmed by cell-level experimental analyses. We propose a model for electron flow from sulfide to oxygen that involves periplasmic cytochromes, yet-unidentified conductive periplasmic fibers, and periplasmic oxygen reduction. This model proposes that an active cable bacterium gains energy in the anodic, sulfide-oxidizing cells, whereas cells in the oxic zone flare off electrons through intense cathodic oxygen respiration without energy conservation; this peculiar form of multicellularity seems unparalleled in the microbial world.

Cable bacteria at oxygen-releasing roots of aquatic plants: a widespread and diverse plant-microbe association.

Cable bacteria are sulfide-oxidising, filamentous bacteria that reduce toxic sulfide levels, suppress methane emissions and drive nutrient and carbon cycling in sediments. Recently, cable bacteria have been found associated with roots of aquatic plants and rice (Oryza sativa). However, the extent to which cable bacteria are associated with aquatic plants in nature remains unexplored. Using newly generated and public 16S rRNA gene sequence datasets combined with fluorescence in situ hybridisation, we investigated the distribution of cable bacteria around the roots of aquatic plants, encompassing seagrass (including seagrass seedlings), rice, freshwater and saltmarsh plants. Diverse cable bacteria were found associated with roots of 16 out of 28 plant species and at 36 out of 55 investigated sites, across four continents. Plant-associated cable bacteria were confirmed across a variety of ecosystems, including marine coastal environments, estuaries, freshwater streams, isolated pristine lakes and intensive agricultural systems. This pattern indicates that this plant-microbe relationship is globally widespread and neither obligate nor species specific. The occurrence of cable bacteria in plant rhizospheres may be of general importance to vegetation vitality, primary productivity, coastal restoration practices and greenhouse gas balance of rice fields and wetlands.

In vitro single-cell dissection revealing the interior structure of cable bacteria.

Filamentous Desulfobulbaceae bacteria were recently discovered as long-range transporters of electrons from sulfide to oxygen in marine sediments. The long-range electron transfer through these cable bacteria has created considerable interests, but it has also raised many questions, such as what structural basis will be required to enable micrometer-sized cells to build into centimeter-long continuous filaments? Here we dissected cable bacteria cells in vitro by atomic force microscopy and further explored the interior, which is normally hidden behind the outer membrane. Using nanoscale topographical and mechanical maps, different types of bacterial cell-cell junctions and strings along the cable length were identified. More important, these strings were found to be continuous along the bacterial cells passing through the cell-cell junctions. This indicates that the strings serve an important function in maintaining integrity of individual cable bacteria cells as a united filament. Furthermore, ridges in the outer membrane are found to envelop the individual strings at cell-cell junctions, and they are proposed to strengthen the junctions. Finally, we propose a model for the division and growth of the cable bacteria, which illustrate the possible structural requirements for the formation of centimeter-length filaments in the recently discovered cable bacteria.

Long-distance electron transport in individual, living cable bacteria.

Electron transport within living cells is essential for energy conservation in all respiring and photosynthetic organisms. While a few bacteria transport electrons over micrometer distances to their surroundings, filaments of cable bacteria are hypothesized to conduct electric currents over centimeter distances. We used resonance Raman microscopy to analyze cytochrome redox states in living cable bacteria. Cable-bacteria filaments were placed in microscope chambers with sulfide as electron source and oxygen as electron sink at opposite ends. Along individual filaments a gradient in cytochrome redox potential was detected, which immediately broke down upon removal of oxygen or laser cutting of the filaments. Without access to oxygen, a rapid shift toward more reduced cytochromes was observed, as electrons were no longer drained from the filament but accumulated in the cellular cytochromes. These results provide direct evidence for long-distance electron transport in living multicellular bacteria.

Protein Nanowires: the Electrification of the Microbial World and Maybe Our Own.

Electrically conductive protein nanowires appear to be widespread in the microbial world and are a revolutionary "green" material for the fabrication of electronic devices. Electrically conductive pili (e-pili) assembled from type IV pilin monomers have independently evolved multiple times in microbial history as have electrically conductive archaella (e-archaella) assembled from homologous archaellin monomers. A role for e-pili in long-range (micrometer) extracellular electron transport has been demonstrated in some microbes. The surprising finding of e-pili in syntrophic bacteria and the role of e-pili as conduits for direct interspecies electron transfer have necessitated a reassessment of routes for electron flux in important methanogenic environments, such as anaerobic digesters and terrestrial wetlands. Pilin monomers similar to those found in e-pili may also be a major building block of the conductive "cables" that transport electrons over centimeter distances through continuous filaments of cable bacteria consisting of a thousand cells or more. Protein nanowires harvested from microbes have many functional and sustainability advantages over traditional nanowire materials and have already yielded novel electronic devices for sustainable electricity production, neuromorphic memory, and sensing. e-pili can be mass produced with an Escherichia coli chassis, providing a ready source of material for electronics as well as for studies on the basic mechanisms for long-range electron transport along protein nanowires. Continued exploration is required to better understand the electrification of microbial communities with microbial nanowires and to expand the "green toolbox" of sustainable materials for wiring and powering the emerging "Internet of things."

A Cross-System Comparison of Dark Carbon Fixation in Coastal Sediments.

Dark carbon fixation (DCF) by chemoautotrophic microorganisms can sustain food webs in the seafloor by local production of organic matter independent of photosynthesis. The process has received considerable attention in deep sea systems, such as hydrothermal vents, but the regulation, depth distribution, and global importance of coastal sedimentary DCF have not been systematically investigated. Here we surveyed eight coastal sediments by means of stable isotope probing (13C-DIC) combined with bacterial biomarkers (phospholipid-derived fatty acids) and compiled additional rates from literature into a global database. DCF rates in coastal sediments range from 0.07 to 36.30 mmol C m-2 day-1, and there is a linear relation between DCF and water depth. The CO2 fixation ratio (DCF/CO2 respired) also shows a trend with water depth, decreasing from 0.09 in nearshore environments to 0.04 in continental shelf sediments. Five types of depth distributions of chemoautotrophic activity are identified based on the mode of pore water transport (advective, bioturbated, and diffusive) and the dominant pathway of microbial sulfur oxidation. Extrapolated to the global coastal ocean, we estimate a DCF rate of 0.04 to 0.06 Pg C year-1, which is less than previous estimates based on indirect measurements (0.15 Pg C year-1), but remains substantially higher than the global DCF rate at deep sea hydrothermal vents (0.001-0.002 Pg C year-1).

Microbial diversity and functional response to the redox dynamics of pyrite-rich sediment and the impact of preload surcharge.

Microbial diversity and activities play pivotal biogeochemical roles in a redox-sensitive, pyrite-rich sediment's ecosystem. However, very little is known about the microbial community composition and distribution among the redox zones of pyrite-rich sediment and their response to changes caused by the burial of the sediment beneath compacted fill. In the present work, culture-independent, molecular phylogenetic investigations of the prokaryotic population and its diversity in a naturally occurring pyrite-rich sediment were undertaken to determine the microbial community composition, richness, diversity and distributions among the varying redox zones and their functional response to the imposition of surface surcharge, in the form of compacted fill. It was established that the pyrite-rich sediment is a redox-sensitive environment consisting of microhabitats with distinct and discontinuous physico-chemical characteristics, including DO, pH, Eh, temperature, electrical conductivity and salinity. It is a favourable environment for cyclic transformation of inorganic sulphur compounds and a unique environment for the habitation and growth of various microorganisms. Microbes adapted to the microhabitat and lived together in consortia, in response to their physiological and functional requirements. Microbes involved in the sulphur cycle had their populations concentrated in the oxic zone, while those involved in iron and carbon cycles were prevalent in the anoxic zones. As a result, highly diverse microbial populations occurred in isolated peaks within the sediment. The physico-chemical differences within the sediment changed in response to changes in the sediment redox dynamics. Imposition of the surcharge resulted in significant changes in the pH, temperature, Eh, DO, EC and salinity, reflecting marked re-distribution of the microbial population within the ecosystem. The cable bacteria phenomenon was evident in the sediment studied; however, there were doubt regarding their filamentous occurrence.

Cable bacteria generate a firewall against euxinia in seasonally hypoxic basins.

Seasonal oxygen depletion (hypoxia) in coastal bottom waters can lead to the release and persistence of free sulfide (euxinia), which is highly detrimental to marine life. Although coastal hypoxia is relatively common, reports of euxinia are less frequent, which suggests that certain environmental controls can delay the onset of euxinia. However, these controls and their prevalence are poorly understood. Here we present field observations from a seasonally hypoxic marine basin (Grevelingen, The Netherlands), which suggest that the activity of cable bacteria, a recently discovered group of sulfur-oxidizing microorganisms inducing long-distance electron transport, can delay the onset of euxinia in coastal waters. Our results reveal a remarkable seasonal succession of sulfur cycling pathways, which was observed over multiple years. Cable bacteria dominate the sediment geochemistry in winter, whereas, after the summer hypoxia, Beggiatoaceae mats colonize the sediment. The specific electrogenic metabolism of cable bacteria generates a large buffer of sedimentary iron oxides before the onset of summer hypoxia, which captures free sulfide in the surface sediment, thus likely preventing the development of bottom water euxinia. As cable bacteria are present in many seasonally hypoxic systems, this euxinia-preventing firewall mechanism could be widely active, and may explain why euxinia is relatively infrequently observed in the coastal ocean.

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

Seasonal hypoxia in coastal systems drastically changes the availability of electron acceptors in bottom water, which alters the sedimentary reoxidation of reduced compounds. However, the effect of seasonal hypoxia on the chemolithoautotrophic community that catalyzes these reoxidation reactions is rarely studied. Here, we examine the changes in activity and structure of the sedimentary chemolithoautotrophic bacterial community of a seasonally hypoxic saline basin under oxic (spring) and hypoxic (summer) conditions. Combined 16S rRNA gene amplicon sequencing and analysis of phospholipid-derived fatty acids indicated a major temporal shift in community structure. Aerobic sulfur-oxidizing Gammaproteobacteria (Thiotrichales) and Epsilonproteobacteria (Campylobacterales) were prevalent during spring, whereas Deltaproteobacteria (Desulfobacterales) related to sulfate-reducing bacteria prevailed during summer hypoxia. Chemolithoautotrophy rates in the surface sediment were three times higher in spring than in summer. The depth distribution of chemolithoautotrophy was linked to the distinct sulfur oxidation mechanisms identified through microsensor profiling, i.e., canonical sulfur oxidation, electrogenic sulfur oxidation by cable bacteria, and sulfide oxidation coupled to nitrate reduction by Beggiatoaceae The metabolic diversity of the sulfur-oxidizing bacterial community suggests a complex niche partitioning within the sediment, probably driven by the availability of reduced sulfur compounds (H2S, S0, and S2O32-) and electron acceptors (O2 and NO3-) regulated by seasonal hypoxia.IMPORTANCE Chemolithoautotrophic microbes in the seafloor are dependent on electron acceptors, like oxygen and nitrate, that diffuse from the overlying water. Seasonal hypoxia, however, drastically changes the availability of these electron acceptors in the bottom water; hence, one expects a strong impact of seasonal hypoxia on sedimentary chemolithoautotrophy. A multidisciplinary investigation of the sediments in a seasonally hypoxic coastal basin confirms this hypothesis. Our data show that bacterial community structure and chemolithoautotrophic activity varied with the seasonal depletion of oxygen. Unexpectedly, the dark carbon fixation was also dependent on the dominant microbial pathway of sulfur oxidation occurring in the sediment (i.e., canonical sulfur oxidation, electrogenic sulfur oxidation by cable bacteria, and sulfide oxidation coupled to nitrate reduction by Beggiatoaceae). These results suggest that a complex niche partitioning within the sulfur-oxidizing bacterial community additionally affects the chemolithoautotrophic community of seasonally hypoxic sediments.

Electrogenic sulfur oxidation in a northern saltmarsh (St. Lawrence Estuary, Canada).

Measurements of porewater O2, pH, and H2S microprofiles in intact sediment cores collected in a northern saltmarsh in the St. Lawrence Estuary (Quebec, Canada) revealed the occurrence of electrogenic sulfur oxidation (e-SOx) by filamentous "cable" bacteria in submerged marsh pond sediments in the high marsh. In summer, the geochemical fingerprint of e-SOx was apparent in intact cores, while in fall, cable bacteria were detected by fluorescence in situ hybridization and the characteristic geochemical signature of e-SOx was observed only upon prolonged incubation. In exposed, unvegetated creek bank sediments sampled in the low marsh in summer, cable bacteria developed only in repacked cores of sieved (500 µm), homogenized sediments. These results suggest that e-SOx is suppressed by the activity of macrofauna in exposed, unvegetated marsh sediments. A reduced abundance of benthic invertebrates may promote e-SOx development in marsh ponds, which are dominant features of subarctic saltmarshes as in the St. Lawrence Estuary.

Effects of cable bacteria on vertical redox profile formation and phenanthrene biodegradation in intertidal sediment responded to tide.

Periodic oxygen permeation is critical for pollutant removal within intertidal sediments. However, tidal effects on the vertical redox profile associated with cable bacterial activity is not well understood. In this study, we simulated and quantified the effects of tidal flooding, exposing, and their periodic alternation on vertical redox reactions and phenanthrene removal driven by cable bacteria in the riverbank sediment. Results show that electrogenic sulfur oxidation (e-SOx) mediated by cable bacteria during exposing process drove the vertical permeation of oxidation potential characterized by a decrease in Fe(II) and sulfide concentrations. The sulfate produced was observed in deep sediment (5-10 mm) and served as an electron acceptor for anaerobic oxidation, thereby triggering the functional succession of microbial community. About 78.2 % and 80.8 % of phenanthrene was degraded in deep sediment where cable bacteria grew well under exposing and tidal conditions. Anaerobic processes during tidal flood were also found to be important for the survival of cable bacteria. Higher cable bacteria abundance (up to 1.5 %) was observed under tidal conditions compared to that under continuous exposing conditions and flooding conditions. This might be attributed to lower oxidation stress and sulfide replenishment via sulfate reduction while flooding. Under tidal conditions, the cable bacteria interacted with sulfate reduction bacteria (e.g. Desulfobacca spp. and Desulfatiglans spp.) and maintained the dynamic balance of HS- and SO42- in sediment profiles. This HS--SO42- cycle could serve as a "redox connector" that continuously delivers oxidation potential to deep sediments, resulting in the removal of organic pollutants. The findings provide preliminary evidence of the self-purification mechanisms within intertidal sediments and suggest a potential strategy for sediment remediation.

Electromicrobiological concentration cells are an overlooked potential energy conservation mechanism for subsurface microorganisms.

Thermodynamics has predicted many different kinds of microbial metabolism by determining which pairs of electron acceptors and donors will react to produce an exergonic reaction (a negative net change in Gibbs free energy). In energy-limited environments, such as the deep subsurface, such an approach can reveal the potential for unexpected or counter-intuitive energy sources for microbial metabolism. Up until recently, these thermodynamic calculations have been carried out with the assumption that chemical species appearing on the reactant and product side of a reaction formula have a constant concentration, and thus do not count towards net concentration changes and the overall direction of the reaction. This assumption is reasonable considering microorganisms are too small (~1 µm) for any significant differences in concentration to overcome diffusion. However, recent discoveries have demonstrated that the reductive and oxidative halves of reactions can be separated by much larger distances, from millimetres to centimetres via conductive filamentous bacteria, mineral conductivity, and biofilm conductivity. This means that the concentrations of reactants and products can indeed be different, and that concentration differences can contribute to the net negative change in Gibbs free energy. It even means that the same redox reaction, simultaneously running in forward and reverse, can drive energy conservation, in an ElectroMicrobiological Concentration Cell (EMCC). This paper presents a model to investigate this phenomenon and predict under which circumstances such concentration-driven metabolism might take place. The specific cases of oxygen concentration cells, sulfide concentration cells, and hydrogen concentration cells are examined in more detail.

First single-strain enrichments of Electrothrix cable bacteria, description of E. aestuarii sp. nov. and E. rattekaaiensis sp. nov., and proposal of a cable bacteria taxonomy following the rules of the SeqCode.

Cable bacteria are electrically conductive, filamentous Desulfobulbaceae, which are morphologically, functionally, and phylogenetically distinct from the other members of this family. Cable bacteria have not been obtained in pure culture and were therefore previously described as candidate genera, Candidatus Electrothrix and Ca. Electronema; a representative of the latter is available as single-strain sediment enrichment. Here we present an improved workflow to obtain the first single-strain enrichments of Ca. Electrothrix and report their metagenome-assembled genomes (MAGs) and morphology. Based on these results and on previously published high-quality MAGs and morphological data of cable bacteria from both candidate genera, we propose to adopt the genus names Electrothrix and Electronema following the rules of the Code of Nomenclature of Prokaryotes Described from Sequence Data (SeqCode), with Electrothrix communis RBTS and Electronema aureum GSTS, respectively, as the nomenclatural types of the genera. Furthermore, based on average nucleotide identity (ANI) values < 95 % with any described species, we propose two of our three single-strain enrichment cultures as novel species of the genus Electrothrix, with the names E. aestuarii sp. nov. and E. rattekaaiensis sp. nov., according to the SeqCode.

Cable bacteria delay euxinia and modulate phosphorus release in coastal hypoxic systems.

Cable bacteria are long, filamentous bacteria with a unique metabolism involving centimetre-scale electron transport. They are widespread in the sediment of seasonally hypoxic systems and their metabolic activity stimulates the dissolution of iron sulfides (FeS), releasing large quantities of ferrous iron (Fe2+) into the pore water. Upon contact with oxygen, Fe2+ oxidation forms a layer of iron(oxyhydr)oxides (FeOx), which in its turn can oxidize free sulfide (H2S) and trap phosphorus (P) diffusing upward. The metabolism of cable bacteria could thus prevent the release of H2S from the sediment and reduce the risk of euxinia, while at the same time modulating P release over seasonal timescales. However, experimental support for this so-called 'iron firewall hypothesis' is scarce. Here, we collected natural sediment in a seasonally hypoxic basin in three different seasons. Undisturbed sediment cores were incubated under anoxic conditions and the effluxes of H2S, dissolved iron (dFe) and phosphate (PO4 3-) were monitored for up to 140 days. Cores with recent cable bacterial activity revealed a high stock of sedimentary FeOx, which delayed the efflux of H2S for up to 102 days. Our results demonstrate that the iron firewall mechanism could exert an important control on the prevalence of euxinia and regulate the P release in coastal oceans.

Cable bacteria: widespread filamentous electroactive microorganisms protecting environments.

Cable bacteria have been identified and detected worldwide since their discovery in marine sediments in Aarhus Bay, Denmark. Their activity can account for the majority of oxygen consumption and sulfide depletion in sediments, and they induce sulfate accumulation, pH excursions, and the generation of electric fields. In addition, they can affect the fluxes of other elements such as calcium, iron, manganese, nitrogen, and phosphorous. Recent developments in our understanding of the impact of cable bacteria on element cycling have revealed their positive contributions to mitigating environmental problems, such as recovering self-purification capacity, enhancing petroleum hydrocarbon degradation, alleviating phosphorus eutrophication, delaying euxinia, and reducing methane emission. We highlight recent research outcomes on their distribution, state-of-the-art findings on their physiological characteristics, and ecological contributions.