Insights into the genome of large sulfur bacteria revealed by analysis of single filaments.
Marine sediments are frequently covered by mats of the filamentous Beggiatoa and other large nitrate-storing bacteria that oxidize hydrogen sulfide using either oxygen or nitrate, which they store in intracellular vacuoles. Despite their conspicuous metabolic properties and their biogeochemical importance, little is known about their genetic repertoire because of the lack of pure cultures. Here, we present a unique approach to access the genome of single filaments of Beggiatoa by combining whole genome amplification, pyrosequencing, and optical genome mapping. Sequence assemblies were incomplete and yielded average contig sizes of approximately 1 kb. Pathways for sulfur oxidation, nitrate and oxygen respiration, and CO2 fixation confirm the chemolithoautotrophic physiology of Beggiatoa. In addition, Beggiatoa potentially utilize inorganic sulfur compounds and dimethyl sulfoxide as electron acceptors. We propose a mechanism of vacuolar nitrate accumulation that is linked to proton translocation by vacuolar-type ATPases. Comparative genomics indicates substantial horizontal gene transfer of storage, metabolic, and gliding capabilities between Beggiatoa and cyanobacteria. These capabilities enable Beggiatoa to overcome non-overlapping availabilities of electron donors and acceptors while gliding between oxic and sulfidic zones. The first look into the genome of these filamentous sulfur-oxidizing bacteria substantially deepens the understanding of their evolution and their contribution to sulfur and nitrogen cycling in marine sediments.
Mussmann
Marc
M
Max Planck Institute for Marine Microbiology, Bremen, Germany. mussmann@mpi-bremen.de
Hu
Fen Z
FZ
Richter
Michael
M
de Beer
Dirk
D
Preisler
André
A
Jørgensen
Bo B
BB
Huntemann
Marcel
M
Glöckner
Frank Oliver
FO
Amann
Rudolf
R
Koopman
Werner J H
WJ
Lasken
Roger S
RS
Janto
Benjamin
B
Hogg
Justin
J
Stoodley
Paul
P
Boissy
Robert
R
Ehrlich
Garth D
GD
D008841:Actin Cytoskeleton / Q000235:genetics*; D001483:Base Sequence; D053524:Beggiatoa / Q000235:genetics*; D016680:Genome, Bacterial; D006862:Hydrogen Sulfide / Q000378:metabolism; D053858:Metabolic Networks and Pathways / Q000235:genetics*; D009566:Nitrates / Q000378:metabolism; D010084:Oxidation-Reduction; D010100:Oxygen / Q000378:metabolism
D009566:Nitrates; D010100:Oxygen; D006862:Hydrogen Sulfide