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Groundwater cable bacteria conserve energy by sulfur disproportionation.

ABSTRACT: Cable bacteria of the family Desulfobulbaceae couple spatially separated sulfur oxidation and oxygen or nitrate reduction by long-distance electron transfer, which can constitute the dominant sulfur oxidation process in shallow sediments. However, it remains unknown how cells in the anoxic part of the centimeter-long filaments conserve energy. We found 16S rRNA gene sequences similar to groundwater cable bacteria in a 1-methylnaphthalene-degrading culture (1MN). Cultivation with elemental sulfur and thiosulfate with ferrihydrite or nitrate as electron acceptors resulted in a first cable bacteria enrichment culture dominated >90% by 16S rRNA sequences belonging to the Desulfobulbaceae. Desulfobulbaceae-specific fluorescence in situ hybridization (FISH) unveiled single cells and filaments of up to several hundred micrometers length to belong to the same species. The Desulfobulbaceae filaments also showed the distinctive cable bacteria morphology with their continuous ridge pattern as revealed by atomic force microscopy. The cable bacteria grew with nitrate as electron acceptor and elemental sulfur and thiosulfate as electron donor, but also by sulfur disproportionation when Fe(Cl)2 or Fe(OH)3 were present as sulfide scavengers. Metabolic reconstruction based on the first nearly complete genome of groundwater cable bacteria revealed the potential for sulfur disproportionation and a chemo-litho-autotrophic metabolism. The presence of different types of hydrogenases in the genome suggests that they can utilize hydrogen as alternative electron donor. Our results imply that cable bacteria not only use sulfide oxidation coupled to oxygen or nitrate reduction by LDET for energy conservation, but sulfur disproportionation might constitute the energy metabolism for cells in large parts of the cable bacterial filaments.

SUBMITTER: Muller H

PROVIDER: S-EPMC6976610 | biostudies-literature | 2020 Feb

REPOSITORIES: biostudies-literature

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Groundwater cable bacteria conserve energy by sulfur disproportionation.

Müller Hubert H Marozava Sviatlana S Probst Alexander J AJ Meckenstock Rainer U RU

The ISME journal 20191114 2

Cable bacteria of the family Desulfobulbaceae couple spatially separated sulfur oxidation and oxygen or nitrate reduction by long-distance electron transfer, which can constitute the dominant sulfur oxidation process in shallow sediments. However, it remains unknown how cells in the anoxic part of the centimeter-long filaments conserve energy. We found 16S rRNA gene sequences similar to groundwater cable bacteria in a 1-methylnaphthalene-degrading culture (1MN). Cultivation with elemental sulfur ...[more]

PMID: 31728021

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Project description:Cable bacteria are multicellular sulfide oxidizing bacteria that display a unique metabolism based on long-distance electron transport. Cells in deeper sediment layers perform the sulfide oxidizing half-reaction whereas cells in the surface layers of the sediment perform the oxygen-reducing half-reaction. These half-reactions are coupled via electron transport through a conductive fiber network that runs along the shared cell envelope. Remarkably, only the sulfide oxidizing half-reaction is coupled to biosynthesis and growth whereas the oxygen reducing half-reaction serves to rapidly remove electrons from the conductive fiber network and is not coupled to energy generation and growth. Cells residing in the oxic zone are believed to (temporarily) rely on storage compounds of which polyphosphate (poly-P) is prominently present in cable bacteria. Here we investigate the role of poly-P in the metabolism of cable bacteria within the different redox environments. To this end, we combined nanoscale secondary ion mass spectrometry with dual-stable isotope probing (13C-DIC and 18O-H2O) to visualize the relationship between growth in the cytoplasm (13C-enrichment) and poly-P activity (18O-enrichment). We found that poly-P was synthesized in almost all cells, as indicated by 18O enrichment of poly-P granules. Hence, poly-P must have an important function in the metabolism of cable bacteria. Within the oxic zone of the sediment, where little growth is observed, 18O enrichment in poly-P granules was significantly lower than in the suboxic zone. Thus, both growth and poly-P metabolism appear to be correlated to the redox environment. However, the poly-P metabolism is not coupled to growth in cable bacteria, as many filaments from the suboxic zone showed poly-P activity but did not grow. We hypothesize that within the oxic zone, poly-P is used to protect the cells against oxidative stress and/or as a resource to support motility, while within the suboxic zone, poly-P is involved in the metabolic regulation before cells enter a non-growing stage.

Project description:BackgroundBiofilms in sulfide-rich springs present intricate microbial communities that play pivotal roles in biogeochemical cycling. We studied chemoautotrophically based biofilms that host diverse CPR bacteria and grow in sulfide-rich springs to investigate microbial controls on biogeochemical cycling.ResultsSulfide springs biofilms were investigated using bulk geochemical analysis, genome-resolved metagenomics, and scanning transmission X-ray microscopy (STXM) at room temperature and 87 K. Chemolithotrophic sulfur-oxidizing bacteria, including Thiothrix and Beggiatoa, dominate the biofilms, which also contain CPR Gracilibacteria, Absconditabacteria, Saccharibacteria, Peregrinibacteria, Berkelbacteria, Microgenomates, and Parcubacteria. STXM imaging revealed ultra-small cells near the surfaces of filamentous bacteria that may be CPR bacterial episymbionts. STXM and NEXAFS spectroscopy at carbon K and sulfur L2,3 edges show that filamentous bacteria contain protein-encapsulated spherical elemental sulfur granules, indicating that they are sulfur oxidizers, likely Thiothrix. Berkelbacteria and Moranbacteria in the same biofilm sample are predicted to have a novel electron bifurcating group 3b [NiFe]-hydrogenase, putatively a sulfhydrogenase, potentially linked to sulfur metabolism via redox cofactors. This complex could potentially contribute to symbioses, for example, with sulfur-oxidizing bacteria such as Thiothrix that is based on cryptic sulfur cycling. One Doudnabacteria genome encodes adjacent sulfur dioxygenase and rhodanese genes that may convert thiosulfate to sulfite. We find similar conserved genomic architecture associated with CPR bacteria from other sulfur-rich subsurface ecosystems.ConclusionsOur combined metagenomic, geochemical, spectromicroscopic, and structural bioinformatics analyses of biofilms growing in sulfide-rich springs revealed consortia that contain CPR bacteria and sulfur-oxidizing Proteobacteria, including Thiothrix, and bacteria from a new family within Beggiatoales. We infer roles for CPR bacteria in sulfur and hydrogen cycling. Video Abstract.

Project description:The disproportionation of inorganic sulfur compounds could be widespread in natural habitats, and microorganisms could produce energy to support primary productivity through this catabolism. However, the microorganisms that carry this process out and the catabolic pathways at work remain relatively unstudied. Here, we investigated the bacterial diversity involved in sulfur disproportionation in hydrothermal plumes from Carlsberg Ridge in the northwestern Indian Ocean by enrichment cultures. A bacterial community analysis revealed that bacteria of the genera Sulfurimonas and Sulfurovum, belonging to the phylum Campylobacterota and previously having been characterized as chemolithoautotrophic sulfur oxidizers, were the most dominant members in six enrichment cultures. Subsequent bacterial isolation and physiological studies confirmed that five Sulfurimonas and Sulfurovum isolates could disproportionate thiosulfate and elemental sulfur. The ability to disproportionate sulfur was also demonstrated in several strains of Sulfurimonas and Sulfurovum that were isolated from hydrothermal vents or other natural environments. Dialysis membrane experiments showed that S0 disproportionation did not require the direct contact of cells with bulk sulfur. A comparative genomic analysis showed that Campylobacterota strains did not contain some genes of the Dsr and rDSR pathways (aprAB, dsrAB, dsrC, dsrMKJOP, and qmoABC) that are involved in sulfur disproportionation in some other taxa, suggesting the existence of an unrevealed catabolic pathway for sulfur disproportionation. These findings provide evidence for the catabolic versatility of these Campylobacterota genera, which are widely distributed in chemosynthetic environments, and expand our knowledge of the microbial taxa involved in this reaction of the biogeochemical sulfur cycle in hydrothermal vent environments. IMPORTANCE The phylum Campylobacterota, notably represented by the genera Sulfurimonas and Sulfurovum, is ubiquitous and predominant in deep-sea hydrothermal systems. It is well-known to be the major chemolithoautotrophic sulfur-oxidizing group in these habitats. Herein, we show that the mesophilic predominant chemolithoautotrophs of the genera Sulfurimonas and Sulfurovum could grow via sulfur disproportionation to gain energy. This is the first report of the chemolithoautotrophic disproportionation of thiosulfate and elemental sulfur within the genera Sulfurimonas and Sulfurovum, and this comes in addition to their already known role in the chemolithoautotrophic oxidation of sulfur compounds. Sulfur disproportionation via chemolithoautotrophic Campylobacterota may represent a previously unrecognized primary production process in hydrothermal vent ecosystems.

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Groundwater cable bacteria conserve energy by sulfur disproportionation.

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Groundwater cable bacteria conserve energy by sulfur disproportionation.

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