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Anaerobic ammonium oxidation linked to sulfate and ferric iron reduction fuels nitrogen loss in marine sediments

  • E. Emilia Rios-Del Toro
  • Edgardo I. Valenzuela
  • Nguyen E. López-Lozano
  • M. Guadalupe Cortés-Martínez
  • Miguel A. Sánchez-Rodríguez
  • Omar Calvario-Martínez
  • Salvador Sánchez-Carrillo
  • Francisco J. Cervantes
Original Paper

Abstract

Availability of fixed nitrogen is a pivotal driver on primary productivity in the oceans, thus the identification of key processes triggering nitrogen losses from these ecosystems is of major importance as they affect ecosystems function and consequently global biogeochemical cycles. Denitrification and anaerobic ammonium oxidation coupled to nitrite reduction (Anammox) are the only identified marine sinks for fixed nitrogen. The present study provides evidence indicating that anaerobic ammonium oxidation coupled to the reduction of sulfate, the most abundant electron acceptor present in the oceans, prevails in marine sediments. Tracer analysis with 15N-ammonium revealed that this microbial process, here introduced as Sulfammox, accounts for up to 5 μg 15N2 produced g−1 day−1 in sediments collected from the eastern tropical North Pacific coast. Raman and X-ray diffraction spectroscopies revealed that elemental sulfur and sphalerite (ZnFeS) were produced, besides free sulfide, during the course of Sulfammox. Anaerobic ammonium oxidation linked to Fe(III) reduction (Feammox) was also observed in the same marine sediments accounting for up to 2 μg 15N2 produced g−1 day−1. Taxonomic characterization, based on 16S rRNA gene sequencing, of marine sediments performing the Sulfammox and Feammox processes revealed the microbial members potentially involved. These novel nitrogen sinks may significantly fuel nitrogen loss in marine environments. These findings suggest that the interconnections among the oceanic biogeochemical cycles of N, S and Fe are much more complex than previously considered.

Keywords

Anaerobic ammonium oxidation Iron cycle Marine environment Nitrogen cycle Sulfur cycle 

Notes

Acknowledgements

We thank Andreas Kappler, Alfons Stams, Sonia Arriaga, Frederic Thalasso, Elías Razo-Flores and Miguel Ávalos for discussions. This work was financially supported by grants from the Council of Science and Technology of Mexico (Program Frontiers in Science, Grant 1289) and the Marcos Moshinsky Foundation to FJC. We thank Jaime García-Murillo, Dulce Partida, Juan Pablo Rodas, Beatriz Rivera, Ana Iris Peña, Ma. Carmen Rocha-Medina, Guadalupe Ortega-Salazar, Guillermo Vidriales, and José Luis Ayala for technical support, as well as Rogelio Vázquez for assistance during sediments collection expeditions. We are also grateful with Raquel Sánchez-Andrés for editing the figures presented here. We acknowledge the use of infrastructure of the National laboratories LINAN and LANBAMA at IPICYT. We also thank three anonymous reviewers for their constructive comments and suggestions, which improved our manuscript.

Supplementary material

10532_2018_9839_MOESM1_ESM.docx (244.4 mb)
Supplementary material 1 (DOCX 250292 kb)

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Copyright information

© Springer Nature B.V. 2018

Authors and Affiliations

  • E. Emilia Rios-Del Toro
    • 1
  • Edgardo I. Valenzuela
    • 1
  • Nguyen E. López-Lozano
    • 1
  • M. Guadalupe Cortés-Martínez
    • 1
  • Miguel A. Sánchez-Rodríguez
    • 2
  • Omar Calvario-Martínez
    • 2
  • Salvador Sánchez-Carrillo
    • 3
  • Francisco J. Cervantes
    • 1
  1. 1.División de Ciencias AmbientalesInstituto Potosino de Investigación Científica y Tecnológica (IPICYT)San Luis PotosíMexico
  2. 2.Centro de Investigación en Alimentación y Desarrollo (CIAD-Mazatlán)SinaloaMexico
  3. 3.Museo Nacional de Ciencias Naturales-CSICMadridSpain

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