Long-distance electron transport in individual, living cable bacteria

Bjerg, Jesper Tataru; Boschker, Henricus T. S.; Larsen, Steffen; Berry, David; Schmid, Markus; Millo, Diego; Tataru, Paula; Meysman, Filip J. R.; Wagner, Michael; Nielsen, Lars Peter; Schramm, Andreas

doi:10.1073/pnas.1800367115

Cited by 125 publications

(103 citation statements)

References 25 publications

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“…GS (SI Appendix, Table S5 and Dataset S2). Resonance Raman microscopy showed high abundance of c-type cytochromes in living cable bacteria (18), and these c-type cytochromes were most abundant in the cell envelope, as also revealed by Raman microscopy (SI Appendix, Fig. S5).…”

Section: Cable Bacteria Likely Oxidize Sulfide By Reversal Of the Cansupporting

confidence: 52%

“…recently been demonstrated using resonance Raman microscopy (18); other metabolic traits have only been indirectly inferred from the disappearance of substrates or the appearance of metabolites in the sediment environment. A consistent model for cable bacteria metabolism and intra-and intercellular electron transport is currently lacking, and the evolutionary origin of this unique lifestyle remains unclear.…”

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confidence: 99%

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On the evolution and physiology of cable bacteria

Kjeldsen

Schreiber

Thorup

et al. 2019

Proc. Natl. Acad. Sci. U.S.A.

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157

228

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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.

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Section: Cable Bacteria Likely Oxidize Sulfide By Reversal Of the Cansupporting

confidence: 52%

mentioning

confidence: 99%

On the evolution and physiology of cable bacteria

Kjeldsen

Schreiber

Thorup

et al. 2019

Proc. Natl. Acad. Sci. U.S.A.

Self Cite

157

228

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“…The positioning of the cells along the vertical gradient is aided by the motility of cable bacteria (Malkin and Meysman, 2015;Bjerg et al, 2016). Electrons obtained from the anaerobic oxidation of the reduced sulfur are transported through the chain of cells to the oxygenated top layer of the sediment where they are used to reduce oxygen to water, which has been demonstrated in isolated living cable bacteria in the laboratory (Bjerg et al, 2018). As much as half of the oxygen reduction in these sediments may be attributed to cable bacteria.…”

Section: Cable Bacteria and The Sulfur Cyclementioning

confidence: 99%

Phototrophic marine benthic microbiomes: the ecophysiology of these biological entities

Stal

Bolhuis

Cretoiu

2018

Environmental Microbiology

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Summary Phototrophic biofilms are multispecies, self‐sustaining and largely closed microbial ecosystems. They form macroscopic structures such as microbial mats and stromatolites. These sunlight‐driven consortia consist of a number of functional groups of microorganisms that recycle the elements internally. Particularly, the sulfur cycle is discussed in more detail as this is fundamental to marine benthic microbial communities and because recently exciting new insights have been obtained. The cycling of elements demands a tight tuning of the various metabolic processes and require cooperation between the different groups of microorganisms. This is likely achieved through cell‐to‐cell communication and a biological clock. Biofilms may be considered as a macroscopic biological entity with its own physiology. We review the various components of some marine phototrophic biofilms and discuss their roles in the system. The importance of extracellular polymeric substances (EPS) as the matrix for biofilm metabolism and as substrate for biofilm microorganisms is discussed. We particularly assess the importance of extracellular DNA, horizontal gene transfer and viruses for the generation of genetic diversity and innovation, and for rendering resilience to external forcing to these biological entities.

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“…GS should work in a similar way, but driven by e-SOx, electrons for menaquinone reduction should be delivered from the conducting strings present in the periplasm (2) via, e.g. , the highly expressed periplasmic cytochromes (14, 37) and a hitherto unidentified membrane-bound menaquinone reductase (like, e.g. , the Type I cytochrome c3:menaquinone oxidoreductase protein Qrc found in Desulfovibrio vulgaris Hildenborough (38)).…”

Section: Discussionmentioning

confidence: 99%

Dissimilatory Nitrate Reduction to Ammonium in the Cable BacteriumCa. Electronema Sp. GS

Marzocchi

Thorup

Dam

et al. 2020

Preprint

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Cable bacteria are filamentous Desulfobulbaceae that split the energy-conserving reaction of sulphide oxidation into two half reactions occurring in distinct cells. Cable bacteria can use nitrate, but the reduction pathway is unknown, making it difficult to assess their direct impact on the N-cycle. Here we show that the freshwater cable bacterium Ca. Electronema sp. GS performs dissimilatory nitrate reduction to ammonium (DNRA). 15NO3−-amended sediment with Ca. Electronema sp. GS showed higher rates of DNRA and nitrite production than sediment without Ca. Electronema sp. GS. Electron flux from sulphide oxidation, inferred from electric potential measurements, matched the electron flux needed to drive cable bacteria-mediated nitrate reduction. Ca. Electronema sp. GS expressed a complete nap operon for periplasmic nitrate reduction to nitrite, and genes encoding a periplasmic multiheme cytochrome (pMHC), homolog to a pMHC that can catalyse nitrite reduction to ammonium in Ca. Maribeggiatoa. Phylogenetic analysis suggests that the capacity for DNRA was acquired in multiple events through horizontal gene transfer from different organisms, before cable bacteria split into different salinity niches. The architecture of the nitrate reduction system suggests absence of energy conservation through oxidative phosphorylation, indicating that cable bacteria primarily conserve energy through the half reaction of sulfide oxidation.

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Long-distance electron transport in individual, living cable bacteria

Cited by 125 publications

References 25 publications

On the evolution and physiology of cable bacteria

On the evolution and physiology of cable bacteria

Phototrophic marine benthic microbiomes: the ecophysiology of these biological entities

Dissimilatory Nitrate Reduction to Ammonium in the Cable BacteriumCa. Electronema Sp. GS

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