Major contribution of autotrophy to microbial carbon cycling in the deep North Atlantic’s interior

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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 14C-bicarbonate fixation and 3H-leucine incorporation revealed that microbial DIC fixation is substantial in the mesopelagic water masses, ranging from 0.1 to 56.7 μmol 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.

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 understanding of the dark ocean’s carbon cycle and the role of the microbial communities in the transformation of carbon remains rudimentary (Arístegui 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 (TCA) (Dijkhuizen and Harder, 1995). Measurements of CO2 fixation by heterotrophic bacterioplankton are scarce; however, reports suggest that about 1–8% of the biomass production in heterotrophic Bacteria is derived from anaplerotic reactions (Romanenko, 1964; Sorokin, 1993). The extent of the anaplerotic reactions is largely determined by the availability of labile organic carbon whereas more complex organic carbon sources, such as those dominating the deep-ocean dissolved organic matter (DOM) pool, decrease the need for replenishing reactions in the TCA cycle (Doronia and Trotsenko, 1985). In the dark ocean, organic carbon availability is generally limiting heterotrophic bacterial activity. Hence, anaplerotic reactions likely play only a minor role in deep-sea Bacteria metabolism, although clearly more research needs to be done on this aspect.

While commonly the microbial community of the oxygenated water column of the dark ocean is considered to be heterotrophic, as shown for Archaea and Bacteria taking up amino acids (Ouverney and Fuhrman, 2000; Teira et al., 2006), DI14C fixation might be more common than hitherto assumed, particularly for the abundant Crenarchaeota (Herndl et al., 2005; Hansman et al., 2009). Evidence of a major autotrophic crenarchaeal community in the deep ocean is also provided by the isotopic composition of archaeal lipids from a 600 m deep station in the Pacific indicating that DIC fixation accounts for about 80% of the archaeal carbon uptake (Ingalls et al., 2006).

We determined microbial DIC fixation rates and microbial heterotrophic production in the oxygenated meso- and bathypelagic realm of the North Atlantic along a transect from 65°N to 5°S following the eastern branch of the North Atlantic Deep Water (NADW) and additionally, following the western branch of the NADW from 65°N to 35°N. In this regional analysis, we show that dark ocean DIC fixation is substantially more important in the deep-ocean carbon cycle than hitherto appreciated and not restricted to sub- or anoxic regions of the global ocean.

Section snippets

Sampling

Seawater was sampled from well-defined water masses. A calibrated Seabird SBE9/11+ CTD was used to measure conductivity, temperature, pressure and oxygen. The CTD was fitted with 16 bottles each of 12 dm3 volume. The water masses were identified based on their salinity and temperature characteristics during the downcast. The factory calibration of the conductivity and the oxygen sensor was checked for stability with appropriate reference samples measured on board. Salinity standards and samples

Methodological considerations

We tested a batch of the 14C-bicarbonate for potential contamination with organic 14C. The live incubations (31±8 DPM, n=3) and the formaldehyde-killed controls (23±3 DPM, n=3) in these lab experiments were not significantly different (Mann-Whitney-U test, P<0.2) and were in the same range as the average blank measurements during the cruises (36±22 DPM, n=343). In contrast to an earlier report on the impurity of commercially available 14C-bicarbonate solutions (Williams et al., 1972), this

Summary and conclusions

Dark-ocean DIC fixation amounts to about 15–53% of the phytoplankton-derived POC entering the dark ocean, assuming 30% of export production leaving the euphotic zone. DIC fixation (125–3000 m) ranges from 1 mmol C m−2 d−1, using the model based on our data (Table 2), and 2.5 mmol C m−2 d−1 taking into account the local variability (Table 4). Assuming that this autotrophy is fuelled exclusively by ammonia as an energy source, our measured inorganic carbon fixation of 1–2.5 mmol C m−2 d−1 would result in the

Acknowledgments

We thank the captain and crew of the R/V Pelagia for their support at sea and K. Bakker, J. Hegeman, S. Gonzalez and A. Smit for help during sample processing. Special thanks go to A. Burd for sorting out the POC flux model calculations. We acknowledge the constructive comments of anonymous reviewers on a former draft of the manuscript. This work was supported by grants of the Dutch Science Foundation NWO to G.J.H.

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