Giant Hydrogen Sulfide Plume in the Oxygen Minimum Zone off Peru Supports Chemolithoautotrophy

Harald Schunck,Tobias Großkopf,Ruth A Schmitz,Gaute Lavik,Markus B Schilhabel,Moritz Holtappels,Michelle Graco,Julie Laroche,Tim Kalvelage,Philip Rosenstiel,Dhwani K Desai,Sergio Contreras,Herbert Siegel,Marcel M M Kuypers,Carolin R Löscher,Aurélien Paulmier

doi:10.1371/journal.pone.0068661

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 km2, which contained ∼2.2×104 tons of H2S. This was the first time that H2S was measured in the Peruvian OMZ and with ∼440 km3 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.

Highlights

IntroductionCombined with large-scale ocean circulation patterns and poor ventilation of intermediate waters with the ocean surface, the remineralization of rich organic matter leads to oxygen-depleted zones of varying intensities [7,8,9,10]
Eastern Boundary Upwelling Systems are found along the westward shelves of the continents in both the Atlantic and the Pacific Ocean
The total area affected by H2S may have been even larger, as we did not map the extent of the sulfidic plume into the protected area of the Paracas National Reserve

Summary

Introduction

Combined with large-scale ocean circulation patterns and poor ventilation of intermediate waters with the ocean surface, the remineralization of rich organic matter leads to oxygen-depleted zones of varying intensities [7,8,9,10]. These oxygen-depleted waters, referred to as oxygen minimum zones (OMZs), are found in the eastern tropical North and South Pacific, and to a lesser extent in the eastern tropical North and South Atlantic [11]. In addition to OMZs found in regions of strong upwelling, oxygen-depleted waters are present in the northern Indian Ocean and in enclosed basins like the Baltic and the Black Sea [12]

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Results

Conclusion