Geobiology (2006), 4, 123–136 © 2006 The Authors Journal compilation © 2006 Blackwell publishing Ltd 123 Blackwell Publishing Ltd ORIGINAL ARTICLE Microbial fuel cell energy from an ocean cold seep Microbial fuel cell energy from an ocean cold seep C. E. REIMERS, 1 P. GIRGUIS, 2,3 H. A. STECHER III, 1 L. M. TENDER, 4 N. RYCKELYNCK 1 AND P. WHALING 2 1 Hatfield Marine Science Center and College of Oceanic and Atmospheric Sciences, Oregon State University, Newport, Oregon, USA 2 Monterey Bay Aquarium Research Institute, Moss Landing, California, USA 3 Biological Laboratories, Harvard University, Cambridge, Massachusetts, USA 4 Naval Research Laboratory, Center for Bio/Molecular Science and Engineering, Washington DC, USA ABSTRACT Benthic microbial fuel cells are devices that generate modest levels of electrical power in seafloor environments by a mechanism analogous to the coupled biogeochemical reactions that transfer electrons from organic carbon through redox intermediates to oxygen. Two benthic microbial fuel cells were deployed at a deep-ocean cold seep within Monterey Canyon, California, and were monitored for 125 days. Their anodes consisted of single graphite rods that were placed within microbial mat patches of the seep, while the cathodes consisted of carbon- fibre/titanium wire brushes attached to graphite plates suspended ∼0.5 m above the sediment. Power records demonstrated a maximal sustained power density of 34 mW·m -2 of anode surface area, equating to 1100 mW m -2 of seafloor. Molecular phylogenetic analyses of microbial biofilms that formed on the electrode surfaces revealed changes in microbial community composition along the anode as a function of sediment depth and surrounding geochemistry. Near the sediment surface (20–29 cm depth), the anodic biofilm was dominated by micro- organisms closely related to Desulfuromonas acetoxidans . At horizons 46–55 and 70–76 cm below the sediment–water interface, clone libraries showed more diverse populations, with increasing representation of δ-proteobacteria such as Desulfocapsa and Syntrophus, as well as ε-proteobacteria. Genes from phylotypes related to Pseudomonas dominated the cathode clone library. These results confound ascribing a single electron transport role performed by only a few members of the microbial community to explain energy harvesting from marine sediments. In addition, the microbial fuel cells exhibited slowly decreasing current attributable to a combination of anode passivation and sulfide mass transport limitation. Electron micrographs of fuel cell anodes and laboratory experiments confirmed that sulfide oxidation products can build up on anode surfaces and impede electron transfer. Thus, while cold seeps have the potential to provide more power than neighbouring ocean sediments, the limits of mass transport as well as the proclivity for passivation must be considered when developing new benthic microbial fuel cell designs to meet specific power requirements. Received 17 November 2005; accepted 09 February 2006 Corresponding author: C. E. Reimers. Tel.: 541-867-0220; fax: 541-867-0138; e-mail: creimers@coas.oregonstate.edu. INTRODUCTION Microbial fuel cells are tangible proof that bacteria use organic substrates to produce reducing power and to transfer electrons through exogenous materials to oxidants in the environment (Bennetto et al ., 1983; Schröder et al ., 2003; Ieropoulos et al ., 2005). However, many unanswered questions remain about the basic charge transfer mechanisms of these systems, their time- and environment-dependent behaviour, the roles of different micro-organisms and substrates in electricity production, and how to enhance, balance and maintain electrode reactions to increase power and optimize energy recovery (He et al ., 2005; Liu et al ., 2005). The benthic microbial fuel cell (BMFC) is a field-deployable and uniquely configured microbial fuel cell that relies on the natural redox processes in aqueous sediments. These fuel cells are under development as long-term power sources for auton- omous sensors and acoustic communication devices deployed in fresh and salt water environments (Reimers et al ., 2001; Tender et al ., 2002; Holmes et al ., 2004b; Alberte et al ., 2005). We consider the BMFC mechanism as being analogous to the coupled microbial and chemical reactions yielding