Filamentous giant Beggiatoaceae from the Guaymas Basin are capable of both denitrification and dissimilatory nitrate reduction to ammonium

Charles A. Schutte, Andreas Teske, Barbara J. MacGregor, Verena Salman-Carvalho, Gaute Lavik, Philipp Hach, Dirk de Beer

Research output: Contribution to journalArticlepeer-review

10 Scopus citations

Abstract

Filamentous large sulfur-oxidizing bacteria (FLSB) of the family Beggiatoaceae are globally distributed aquatic bacteria that can control geochemical fluxes from the sediment to the water column through their metabolic activity. FLSB mats from hydrothermal sediments of Guaymas Basin, Mexico, typically have a "fried-egg" appearance, with orange filaments dominating near the center and wider white filaments at the periphery, likely reflecting areas of higher and lower sulfide fluxes, respectively. These FLSB store large quantities of intracellular nitrate that they use to oxidize sulfide. By applying a combination of 15N-labeling techniques and genome sequence analysis, we demonstrate that the white FLSB filaments were capable of reducing their intracellular nitrate stores to both nitrogen gas and ammonium by denitrification and dissimilatory nitrate reduction to ammonium (DNRA), respectively. On the other hand, our combined results show that the orange filaments were primarily capable of DNRA. Microsensor profiles through a laboratory-incubated white FLSB mat revealed a 2- to 3-mm vertical separation between the oxic and sulfidic zones. Denitrification was most intense just below the oxic zone, as shown by the production of nitrous oxide following exposure to acetylene, which blocks nitrous oxide reduction to nitrogen gas. Below this zone, a local pH maximum coincided with sulfide oxidation, consistent with nitrate reduction by DNRA. The balance between internally and externally available electron acceptors (nitrate) and electron donors (reduced sulfur) likely controlled the end product of nitrate reduction both between orange and white FLSB mats and between different spatial and geochemical niches within the white FLSB mat.

Original languageEnglish (US)
Article numbere02860-17
JournalApplied and environmental microbiology
Volume84
Issue number15
DOIs
StatePublished - Aug 1 2018

Bibliographical note

Funding Information:
We thank Nina Dombrowski and Brett Baker for early access to the Beggiatoa sp. bin 4572_84 genome and Gabi Klockgether for her assistance with the nitrogen stable isotope analyses. We also thank Gabi Eickert, Karin Hohmann, Vera Hübner, Anja Niclas, Ines Schröder, and Cäcilia Wigand for their assistance with microsensor construction and cruise preparations. We also thank Mandy Joye and her lab members for organizing an emergency shipment of sorely needed supplies halfway through the cruise, enabling us to continue our work when all of our equipment was trapped in a customs warehouse. This work would not have been possible without the efforts of the captain and crew of R/V Atlantis and DSV Alvin. Funding was provided by NSF (grant number 1357238) and the Max Planck Society

Publisher Copyright:
© 2018 American Society for Microbiology.

Keywords

  • Biogeochemistry
  • DNRA
  • Denitrification
  • Marine microbiology
  • Nitrogen cycle

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