Giant hydrogen sulfide plume in the oxygen minimum zone off Peru supports chemolithoautotrophy

PLoS One. 2013 Aug 21;8(8):e68661. doi: 10.1371/journal.pone.0068661. eCollection 2013.

Abstract

In Eastern Boundary Upwelling Systems nutrient-rich waters are transported to the ocean surface, fuelling high photoautotrophic primary production. Subsequent heterotrophic decomposition of the produced biomass increases the oxygen-depletion at intermediate water depths, which can result in the formation of oxygen minimum zones (OMZ). OMZs can sporadically accumulate hydrogen sulfide (H2S), which is toxic to most multicellular organisms and has been implicated in massive fish kills. During a cruise to the OMZ off Peru in January 2009 we found a sulfidic plume in continental shelf waters, covering an area >5500 km(2), which contained ∼2.2×10(4) tons of H2S. This was the first time that H2S was measured in the Peruvian OMZ and with ∼440 km(3) the largest plume ever reported for oceanic waters. We assessed the phylogenetic and functional diversity of the inhabiting microbial community by high-throughput sequencing of DNA and RNA, while its metabolic activity was determined with rate measurements of carbon fixation and nitrogen transformation processes. The waters were dominated by several distinct γ-, δ- and ε-proteobacterial taxa associated with either sulfur oxidation or sulfate reduction. Our results suggest that these chemolithoautotrophic bacteria utilized several oxidants (oxygen, nitrate, nitrite, nitric oxide and nitrous oxide) to detoxify the sulfidic waters well below the oxic surface. The chemolithoautotrophic activity at our sampling site led to high rates of dark carbon fixation. Assuming that these chemolithoautotrophic rates were maintained throughout the sulfidic waters, they could be representing as much as ∼30% of the photoautotrophic carbon fixation. Postulated changes such as eutrophication and global warming, which lead to an expansion and intensification of OMZs, might also increase the frequency of sulfidic waters. We suggest that the chemolithoautotrophically fixed carbon may be involved in a negative feedback loop that could fuel further sulfate reduction and potentially stabilize the sulfidic OMZ waters.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Bacteria / genetics*
  • Bacteria / isolation & purification
  • Bacteria / metabolism
  • Biomass
  • Carbon Cycle
  • Carbon Dioxide / chemistry
  • Chemoautotrophic Growth / physiology*
  • Cluster Analysis
  • Colloids / chemistry
  • Ecosystem
  • Flow Cytometry / methods
  • Genome, Bacterial
  • Hydrogen Sulfide / chemistry*
  • Nitrogen / chemistry
  • Oxygen / chemistry*
  • Pacific Ocean
  • Peru
  • Phylogeny
  • Seawater / chemistry*
  • Sequence Analysis, DNA
  • Sequence Analysis, RNA
  • Sulfides / chemistry
  • Water Microbiology

Substances

  • Colloids
  • Sulfides
  • Carbon Dioxide
  • Nitrogen
  • Oxygen
  • Hydrogen Sulfide

Grant support

Funding was provided by the WGL-PAKT project ‘REAL’ (Leibniz Association), the Max Planck Society and the Helmholtz Association. The Cluster of Excellence “The Future Ocean” provided structural support. This work is a contribution of the Collaborative Research Centre 754 “climate - biogeochemistry interactions in the tropical oceans” (www.sfb754.de), which is supported by the German Research Association. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.