title: Single-cell Sequencing of Thiomargarita Reveals Genomic Flexibility for Adaptation to Dynamic Redox Conditions.
abstract: Large, colorless sulfur-oxidizing bacteria (LSB) of the family Beggiatoaceae form thick mats at sulfidic sediment surfaces, where they efficiently detoxify sulfide before it enters the water column. The genus Thiomargarita harbors the largest known free-living bacteria with cell sizes of up to 750 μm in diameter. In addition to their ability to oxidize reduced sulfur compounds, some Thiomargarita spp. are known to store large amounts of nitrate, phosphate and elemental sulfur internally. To date little is known about their energy yielding metabolic pathways, and how these pathways compare to other Beggiatoaceae. Here, we present a draft single-cell genome of a chain-forming "Candidatus Thiomargarita nelsonii Thio36", and conduct a comparative analysis to five draft and one full genome of other members of the Beggiatoaceae. "Ca. T. nelsonii Thio36" is able to respire nitrate to both ammonium and dinitrogen, which allows them to flexibly respond to environmental changes. Genes for sulfur oxidation and inorganic carbon fixation confirmed that "Ca. T. nelsonii Thio36" can function as a chemolithoautotroph. Carbon can be fixed via the Calvin-Benson-Bassham cycle, which is common among the Beggiatoaceae. In addition we found key genes of the reductive tricarboxylic acid cycle that point toward an alternative CO2 fixation pathway. Surprisingly, "Ca. T. nelsonii Thio36" also encodes key genes of the C2-cycle that convert 2-phosphoglycolate to 3-phosphoglycerate during photorespiration in higher plants and cyanobacteria. Moreover, we identified a novel trait of a flavin-based energy bifurcation pathway coupled to a Na(+)-translocating membrane complex (Rnf). The coupling of these pathways may be key to surviving long periods of anoxia. As other Beggiatoaceae "Ca. T. nelsonii Thio36" encodes many genes similar to those of (filamentous) cyanobacteria. In summary, the genome of "Ca. T. nelsonii Thio36" provides additional insight into the ecology of giant sulfur-oxidizing bacteria, and reveals unique genomic features for the Thiomargarita lineage within the Beggiatoaceae.
authors.affiliation: Molecular Ecology Group, Department of Molecular Ecology, Max Planck Institute for Marine MicrobiologyBremen, Germany; Section Geomicrobiology, GFZ German Research Centre for Geoscience, Helmholtz Centre PotsdamPotsdam, Germany.
authors.forename: Matthias
authors.initials: M
authors.lastname: Winkel
authors.affiliation: HGF MPG Joint Research Group for Deep-sea Ecology and Technology, Max Planck Institute for Marine Microbiology Bremen, Germany.
authors.forename: Verena
authors.initials: V
authors.lastname: Salman-Carvalho
authors.affiliation: Department of Energy Joint Genome Institute, Walnut Creek CA, USA.
authors.forename: Tanja
authors.initials: T
authors.lastname: Woyke
authors.affiliation: Microbial Genomics and Bioinformatics Group, Department of Molecular Ecology, Max Planck Institute for Marine Microbiology Bremen, Germany.
authors.forename: Michael
authors.initials: M
authors.lastname: Richter
authors.affiliation: Leibniz-Institut für Ostseeforschung Warnemünde Rostock, Germany.
authors.forename: Heide N
authors.initials: HN
authors.lastname: Schulz-Vogt
authors.affiliation: Department of Earth Sciences, University of Minnesota, Minneapolis MN, USA.
authors.forename: Beverly E
authors.initials: BE
authors.lastname: Flood
authors.affiliation: Department of Earth Sciences, University of Minnesota, Minneapolis MN, USA.
authors.forename: Jake V
authors.initials: JV
authors.lastname: Bailey
authors.affiliation: Molecular Ecology Group, Department of Molecular Ecology, Max Planck Institute for Marine Microbiology Bremen, Germany.
authors.forename: Marc
authors.initials: M
authors.lastname: Mußmann
keywords: C2-cycle; cyanobacteria; multiple-displacement amplification; single-cell genome; sulfur-oxidizing bacteria; “Candidatus Thiomargarita nelsonii”