Major contribution of autotrophy to microbial carbon cycling in the deep North Atlantic’s interior Thomas Reinthaler a,b,n , Hendrik M. van Aken c , Gerhard J. Herndl a,b a University of Vienna, Department of Marine Biology, Faculty Center of Ecology, Althanstr. 14, 1090 Vienna, Austria b Department of Biological Oceanography, Royal Netherlands Institute for Sea Research (NIOZ), P.O. Box 59, 1790 AB Den Burg, The Netherlands c Department of Physical Oceanography, Royal Netherlands Institute for Sea Research (NIOZ), P.O. Box 59, 1790 AB Den Burg, The Netherlands article info Article history: Received 26 March 2009 Accepted 9 December 2009 Available online 11 March 2010 Keywords: North Atlantic Dark Ocean Chemoautotrophy DIC fixation Heterotrophy Bacteria Archaea abstract Current estimates point to a mismatch of particulate organic carbon supply derived from the surface ocean and the microbial organic carbon demand in the meso- and bathypelagic realm. Based on recent findings that chemoautotrophic Crenarchaeota are abundant in the mesopelagic zone, we quantified dissolved inorganic carbon (DIC) fixation in the meso- and bathypelagic North Atlantic and compared it with heterotrophic microbial activity. Measuring 14 C-bicarbonate fixation and 3 H-leucine incorporation revealed that microbial DIC fixation is substantial in the mesopelagic water masses, ranging from 0.1 to 56.7 mmol C m 3 d 1 , and is within the same order of magnitude as heterotrophic microbial activity. Integrated over the dark ocean’s water column, DIC fixation ranged from 1–2.5 mmol C m 2 d 1 , indicating that chemoautotrophy in the dark ocean represents a significant source of autochthonously produced ‘new organic carbon’ in the ocean’s interior amounting to about 15–53% of the phytoplankton export production. Hence, chemoautotrophic DIC fixation in the oxygenated meso- and bathypelagic water column of the North Atlantic might substantially contribute to the organic carbon demand of the deep-water microbial food web. & 2010 Elsevier Ltd. All rights reserved. 1. Introduction The dark ocean, i.e. below ca. 200 m depth, comprises about 75% of the global ocean’s volume and contains more than 98% of the global dissolved inorganic carbon (DIC) pool (Gruber et al., 2004). While geochemical measurements provide major insights into the general ocean carbon cycle, our mechanistic under- standing of the dark ocean’s carbon cycle and the role of the microbial communities in the transformation of carbon remains rudimentary (Arı ´stegui et al., 2009). The dark ocean harbors around 65% of all pelagic Bacteria and Archaea (Whitman et al., 1998) and a large fraction of the global ocean’s remineralization of organic matter occurs below 200 m depth (Del Giorgio and Duarte, 2002). The generally rapid attenuation with depth of sedimenting particulate organic carbon (POC) (Martin et al., 1987) resulting in low POC inputs, and the constant background of refractory DOC resisting microbial oxidation (Barber, 1968), however, led to the widespread view that microbes in the dark ocean are extremely slow growing or dormant. This view is contradicted by several recent studies showing that microbes in the dark ocean are overall metabolically active (Herndl et al., 2005; Teira et al., 2006, Reinthaler et al., 2006b). Genomic studies on deep-sea microbial communities identified novel genes and metabolic pathways that make it possible for some microbes to thrive as chemoautotrophs on inorganic substrates (Berg et al., 2007; Hallam et al., 2006). Microbial growth in the interior of the ocean is considered to be mainly supported by the organic matter exported from the euphotic zone, with most of the exported particulate and dissolved organic matter remineralized in the mesopelagic zone (Del Giorgio and Duarte, 2002). While the notion that the microbial carbon demand exceeds the particulate organic carbon flux into the dark ocean is not new (Ducklow, 1993; Karl et al., 1988; Simon et al., 1992), recently direct evidence has been presented by comparing biogeochemical carbon flux estimates with microbial activity measurements (Baltar et al., 2009; Reinthaler et al., 2006b). Chemoautotrophy by microbes is common in hypoxic and anoxic environments such as the redox transition zones in the Cariaco Basin, the Black Sea and parts of the central Baltic Sea where uptake of DIC is supported by reduced end-products of anaerobic decomposition (Jost et al., 2008; Karl and Knauer, 1991; Taylor et al., 2001). However, in the oxygenated water column, DIC uptake by the heterotrophic bacterioplankton is generally attributed to anaplerotic reactions in the tricarboxylic acid cycle ARTICLE IN PRESS Contents lists available at ScienceDirect journal homepage: www.elsevier.com/locate/dsr2 Deep-Sea Research II 0967-0645/$ - see front matter & 2010 Elsevier Ltd. All rights reserved. doi:10.1016/j.dsr2.2010.02.023 n Corresponding author at: University of Vienna, Department of Marine Biology, Faculty Center of Ecology, Althanstr. 14, 1090 Vienna, Austria. Tel.: + 43 1 4277 571 02; fax: + 43 1 4277 9571. E-mail address: thomas.reinthaler@univie.ac.at (T. Reinthaler). Deep-Sea Research II 57 (2010) 1572–1580