Original Article

Subject Category: Microbial ecology and functional diversity of natural habitats

The ISME Journal (2014) 8, 1510–1521; doi:10.1038/ismej.2013.246; published online 16 January 2014

Deep-sea hydrothermal vent Epsilonproteobacteria encode a conserved and widespread nitrate reduction pathway (Nap)

Costantino Vetriani1,2,4, James W Voordeckers1,2,4,5, Melitza Crespo-Medina1,2,6, Charles E O'Brien1,2, Donato Giovannelli1,2,3 and Richard A Lutz2

  1. 1Department of Biochemistry and Microbiology, Rutgers University, New Brunswick, NJ, USA
  2. 2Institute of Marine and Coastal Sciences, Rutgers University, New Brunswick, NJ, USA
  3. 3Institute of Marine Science - ISMAR, National Research Council of Italy, CNR, Ancona, Italy

Correspondence: C Vetriani, Institute of Marine and Coastal Sciences, Rutgers University, 71 Dudley Road, New Brunswick, NJ 08901, USA. E-mail: vetriani@marine.rutgers.edu

4These authors contributed equally to this work.

5Current address: Department of Botany and Microbiology, Institute for Environmental Genomics, University of Oklahoma, Norman, OK 73019, USA

6Current address: Department of Biology, East Carolina University, Greenville, NC 27858, USA

Received 14 September 2013; Revised 1 December 2013; Accepted 3 December 2013
Advance online publication 16 January 2014

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Abstract

Despite the frequent isolation of nitrate-respiring Epsilonproteobacteria from deep-sea hydrothermal vents, the genes coding for the nitrate reduction pathway in these organisms have not been investigated in depth. In this study we have shown that the gene cluster coding for the periplasmic nitrate reductase complex (nap) is highly conserved in chemolithoautotrophic, nitrate-reducing Epsilonproteobacteria from deep-sea hydrothermal vents. Furthermore, we have shown that the napA gene is expressed in pure cultures of vent Epsilonproteobacteria and it is highly conserved in microbial communities collected from deep-sea vents characterized by different temperature and redox regimes. The diversity of nitrate-reducing Epsilonproteobacteria was found to be higher in moderate temperature, diffuse flow vents than in high temperature black smokers or in low temperatures, substrate-associated communities. As NapA has a high affinity for nitrate compared with the membrane-bound enzyme, its occurrence in vent Epsilonproteobacteria may represent an adaptation of these organisms to the low nitrate concentrations typically found in vent fluids. Taken together, our findings indicate that nitrate reduction is widespread in vent Epsilonproteobacteria and provide insight on alternative energy metabolism in vent microorganisms. The occurrence of the nap cluster in vent, commensal and pathogenic Epsilonproteobacteria suggests that the ability of these bacteria to respire nitrate is important in habitats as different as the deep-sea vents and the human body.

Keywords:

Epsilonproteobacteria; nitrate reduction; deep-sea vents; napA