Single-cell sequencing of Thiomargarita reveals genomic flexibility for adaptation to dynamic redox conditions

Winkel, Matthias; Salman-Carvalho, Verena; Woyke, Tanja; Richter, Michael; Schulz-Vogt, Heide N.; Flood, Beverly E.; Bailey, Jake V.; Mußmann, Marc

doi:10.3389/fmicb.2016.00964

Title: Single-cell sequencing of Thiomargarita reveals genomic flexibility for adaptation to dynamic redox conditions

Journal Article · Tue Jun 21 00:00:00 EDT 2016 · Frontiers in Microbiology

DOI:https://doi.org/10.3389/fmicb.2016.00964· OSTI ID:1285911

Winkel, Matthias ^[1]; Salman-Carvalho, Verena ^[2]; Woyke, Tanja ^[3]; Richter, Michael ^[4]; Schulz-Vogt, Heide N. ^[5]; Flood, Beverly E. ^[6]; Bailey, Jake V. ^[6]; Mußmann, Marc ^[7]

Max Planck Inst. for Marine Microbiology, Bremen (Germany). Molecular Ecology Group, Dept. of Molecular Ecology; Section Geomicrobiology, GFZ German Research Centre for Geoscience, Helmholtz Centre Potsdam, Potsdam (Germany)
Max Planck Inst. for Marine Microbiology, Bremen (Germany). HGF MPG Joint Research Group for Deep-sea Ecology and Technology
Dept. of Energy Joint Genome Inst., Walnut Creek, CA (United States)
Max Planck Inst. for Marine Microbiology, Bremen (Germany). Microbial Genomics and Bioinformatics Group, Dept. of Molecular Ecology
Leibniz Inst. for Baltic Sea Research, Warnemunde, Rostock (Germany)
Univ. of Minnesota, Minneapolis, MN (United States). Dept. of Earth Sciences
Max Planck Inst. for Marine Microbiology, Bremen (Germany). Molecular Ecology Group, Dept. of Molecular Ecology

© 2016 Winkel, Salman-Carvalho, Woyke, Richter, Schulz-Vogt, Flood, Bailey and Mußmann. 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 CO 2 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.

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Research Organization:: USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States); Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1285911

Alternate ID(s):: OSTI ID: 1378753

Journal Information:: Frontiers in Microbiology, Vol. 7; ISSN 1664-302X

Publisher:: Frontiers Research FoundationCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 24 works

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Major Bottom Water Ventilation Events Do Not Significantly Reduce Basin-Wide Benthic N and P Release in the Eastern Gotland Basin (Baltic Sea) Sommer, Stefan; Clemens, David; Yücel, Mustafa Frontiers in Marine Science, Vol. 4 https://doi.org/10.3389/fmars.2017.00018	journal	February 2017
Chemosynthetic symbiont with a drastically reduced genome serves as primary energy storage in the marine flatworm Paracatenula Jäckle, Oliver; Seah, Brandon K. B.; Tietjen, Målin Proceedings of the National Academy of Sciences, Vol. 116, Issue 17 https://doi.org/10.1073/pnas.1818995116	journal	April 2019

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59 BASIC BIOLOGICAL SCIENCES
"Candidatus Thiomargarita nelsonii"
single-cell genome
sulfur-oxidizing bacteria
cyanobacteria
multiple-displacement amplification
C2-cycle
ribosomal-rna genes
methylococcus-capsulatus bath
electron-transport pathways
colorless sulfur bacteria
marine beggiatoa
energy-conservation
nitrate reductases
draft genome
cold seeps
metabolism

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